Jean-François Lemaître
email: jean-francois.lemaitre@univ-lyon1.fr

Jean-Michel Gaillard

Steven A Ramm

The hidden ageing costs of sperm competition

Keywords:

Ageing and sexual selection are intimately linked. There is by now compelling evidence from studies performed across diverse organisms that males allocating resources to mating competition incur substantial physiological costs, ultimately increasing ageing. However, although insightful, we argue here that to date these studies cover only part of the relationship linking sexual selection and ageing. Crucially, allocation to traits important in post-copulatory sexual selection, i.e. sperm competition, has been largely ignored. As we demonstrate, such allocation could potentially explain much diversity in male and female ageing patterns observed both within and among species. We first review how allocation to sperm competition traits such as sperm and seminal fluid production depends on the quality of resources available to males and can be associated with a wide range of deleterious effects affecting both somatic tissues and the germline, and thus modulate ageing in both survival and reproductive terms. We further hypothesize that common biological features such as plasticity, prudent sperm allocation and seasonality of ejaculate traits might have evolved as counter-adaptations to limit the ageing costs of sperm competition. Finally, we discuss the implications of these emerging ageing costs of sperm competition for current research on the evolutionary ecology of ageing.

INTRODUCTION

The ageing process is generally defined as a progressive decline in the age-specific contribution to fitness [START_REF] Partridge | Optimally, mutation and the evolution of ageing[END_REF]Kowald & Kirkwood 2015;[START_REF] Gaillard | An integrative view of senescence in nature[END_REF], which occurs due to a decrease in fertility and / or survival rates with advancing age (also called reproductive and actuarial senescence, respectively). Age-specific decreases in reproductive performance or survival are widespread in the animal kingdom [START_REF] Nussey | Senescence in natural populations of animals: widespread evidence and its implications for biogerontology[END_REF]Jones et al. 2014), governed by myriad physiological processes [START_REF] López-Otín | The Hallmarks of Aging[END_REF]Kennedy et al. 2014) and potentially largely uncoupled from each other [START_REF] Lemaître | Reproductive senescence: new perspectives in the wild: Reproductive senescence in the wild[END_REF].

The trade-off between growth and reproductive effort early in life, and ageing in terms of reproduction and survivorship constitutes a major cornerstone of our current understanding of the evolution of ageing (Lemaître et al. 2015;Flatt & Partridge 2018). Based on the declining force of natural selection with increasing age [START_REF] Medawar | An unsolved problem of biology[END_REF]), [START_REF] Williams | Pleiotropy, natural selection, and the evolution of senescence[END_REF] proposed the antagonistic pleiotropy theory of ageing, positing that an allele with a positive effect on fitness during early adulthood will be selected even if this same allele is responsible for a decline in reproductive efficiency or survival prospects later in life [START_REF] Williams | Pleiotropy, natural selection, and the evolution of senescence[END_REF][START_REF] Lemaître | Reproductive senescence: new perspectives in the wild: Reproductive senescence in the wild[END_REF]Austad & Hoffman 2018). One physiological mechanism by which the evolutionary trade-off between reproductive effort in early life and ageing can occur is a resource-based allocation trade-off, that constitutes the core of the disposable soma theory of ageing (Kirkwood 1977). This theory postulates that individuals have to allocate the limited resources they acquire to growth, reproduction and somatic maintenance (Kirkwood & Rose 1991). This means that substantial allocation to growth during early life leaves fewer resources to devote to reproduction or somatic maintenance mechanisms (e.g. protein clearance, [START_REF] Vilchez | The role of protein clearance mechanisms in organismal ageing and age-related diseases[END_REF], which is then ultimately responsible for an earlier and/or faster rate of ageing (Kirkwood & Rose 1991;Kirkwood 2017). Another specific physiological pathway, the so-called developmental theory of ageing [START_REF] Maklakov | Evolution of ageing as a tangle of trade-offs: energy versus function[END_REF]) offers an alternative mechanism underlying the genetic trade-off envisioned by [START_REF] Williams | Pleiotropy, natural selection, and the evolution of senescence[END_REF]. According to that theory, physiological processes that allow fast growth and intense reproduction early in life have long-lasting effects that generate pathologies at old ages through cellular hyperfunction [START_REF] Gems | Genetics of longevity in model organisms: debates and paradigm shifts[END_REF]. Decades of research performed under both laboratory and wild conditions support the existence of a trade-off between reproduction and ageing (Flatt & Promislow 2007;Lemaître et al. 2015;Austad & Hoffman 2018).

A striking feature of the many studies investigating the ageing consequences of a strong allocation to reproduction is their overwhelming focus on females (Lemaître et al. 2015). For instance, a first compilation of studies testing for such early-vs. late-life trade-offs in wild populations of vertebrates revealed that 85.3 % of the single-sex studies were focused on females (Lemaître et al. 2015). There are several causes of this bias, including the central role of females in population dynamics, the higher energetic costs of gamete production for females compared to males [START_REF] Hayward | The cost of sex: quantifying energetic investment in gamete production by males and females[END_REF], the obvious physiological costs associated with maternal care (e.g. lactation in harbour seal, Phoca vitulina, Bowen et al. 1992), and the additional need for genetic analyses (and associated uncertainty) when it comes to assigning paternity rather than maternity. Even in laboratory settings where paternity can be assigned more easily, most studies still largely focused on females (but see below). Yet, the recent evidence that the intensity of ageing in both survival (e.g. Lemaître et al. 2020) and reproduction (e.g. Brengdahl et al. 2018) can differ widely between males and females across species strongly emphasizes that we need to investigate how both natural and sexual selection interact to shape male ageing patterns. Such studies could reveal new insights about the evolutionary roots of the sex-specific decline in physiological performance and health issues at late ages [START_REF] Marais | Sex-specific differences in aging and longevity: can sex chromosomes play a role?[END_REF].

So far, all attempts to reconcile male life history strategies within the early-vs. latelife trade-off framework offered by the evolutionary theory of ageing have put forward the predominant role of sexual selection [START_REF] Vinogradov | Male reproductive strategy and decreased longevity[END_REF][START_REF] Promislow | Mate choice, sexual conflict, and evolution of senescence[END_REF]Bonduriansky et al. 2008;[START_REF] Hooper | Sexual competition and the evolution of condition-dependent ageing[END_REF]. Basically, these studies rely on the traditional 'sex role' paradigm in evolutionary ecology (Bateman 1948;[START_REF] Trivers | Parental investment and sexual selection[END_REF], with males competing for gaining access to mating opportunities while females are the choosier sex (Dewsbury 2005;Janicke et al. 2016). Evidence that sexual selection favours conspicuous behaviours and extravagant sexual traits is widespread in nature (Andersson 1994). Moreover, male reproductive effort is known to be associated with some physiological correlates of ageing (e.g. a decrease in antioxidant defences, Alonso-Alvarez et al. 2004, an impaired immune response, [START_REF] Peters | Trade-offs between immune investment and sexual signaling in male mallards[END_REF], or a stronger rate of telomere attrition, [START_REF] Giraudeau | Ageing and the cost of maintaining coloration in the Australian painted dragon[END_REF]. Although the exact physiological pathways linking sexual selection to the degradation of the 'organismal somatic state' are likely to be complex and probably involve a complex role of androgens [START_REF] Alonso-Alvarez | Life history evolution, reproduction, and the origins of sex-dependent aging and longevity[END_REF][START_REF] Metcalf | Why leveraging sex differences in immune tradeoffs may illuminate the evolution of senescence[END_REF], several empirical studies have evidenced an ageing cost of male allocation to sexual competition (see Table 1). Most of these studies have expressed this survival cost in terms of lifespan reduction, which may not directly translate into an ageing cost in the strict sense [START_REF] Péron | Variation in actuarial senescence does not reflect life span variation across mammals[END_REF]). However, a few studies have also considered possible consequences in terms of ageing per se. For instance, in the wild, male red deer (Cervus elaphus) that allocate strongly to reproductive effort by displaying rutting behaviour during an extended period of the breeding season or by controlling large harems suffer from a stronger rate of reproductive ageing, measured through competitive abilities [START_REF] Lemaître | Early life expenditure in sexual competition is associated with increased reproductive senescence in male red deer[END_REF].

Is sperm competition a neglected cause of ageing? Earlier studies have provided important insights into how sexual selection influences lifespan and impacts age-specific reproduction and survival. However, in this perspective article, we argue that studies seeking to decipher the ageing costs of male allocation to sexual competition need to fully embrace its complexity. Specifically, male allocation to sexual competition can be divided into two consecutive episodes: competition over mating (i.e. pre-copulatory competition) and competition over fertilization (i.e. post-copulatory competition) [START_REF] Parker | Sperm competition and the evolution of ejaculates: towards a theory base[END_REF]Andersson & Simmons 2006;Simmons et al. 2017). So far, the physiological and ageing consequences of male allocation to post-copulatory competition have been extensively studied in females (see Box 1 for a synthesis), but remain almost totally overlooked in males, which prevents us from drawing any firm conclusion on how male reproductive allocation influences fitness-related traits in late life.

We thus aim to highlight the untapped potential of sperm competition studies for better understanding the ageing process. As we show, there are multiple ways in which allocation to sperm competition could alter physiological pathways ultimately linked to ageing in reproduction and survivorship (Figure 1). Although other components of the male reproductive phenotype linked to sperm competition success might be considered in the future (e.g. genital morphology; behavioural adaptations), we deliberately focus here on ejaculaterelated adaptations to post-copulatory competition (both sperm and non-sperm components) as these seem likely to be most strongly associated with long-term ageing costs. After considering the various potential costs, conceptually as well as through a critical appraisal of the limited empirical evidence published so far, we further argue that plasticity in many of these traits can best be understood in the light of the evolutionary theory of ageing. Finally, we provide a roadmap for future studies aimed at deciphering the hidden ageing costs of sperm competition.

AGEING COSTS OF SPERM COMPETITION (a) Sperm quantity and quality

Female multiple mating is widespread in nature (Birkhead & Møller 1998). As a consequence, sperm competition (i.e. when sperm from two or more males compete to fertilize a set of ova, [START_REF] Parker | Sperm competition and its evolutionary consequences in the insects[END_REF]) is found in the vast majority of species (Birkhead & Møller 1998). Across species, males can improve their fertilization success through several (nonmutually exclusive) pathways. The most studied pathway is undoubtedly through producing more sperm, as sperm competition game models generally predict that a higher number of sperm within ejaculates provide a fertilization advantage over competitors (reviewed in [START_REF] Pizzari | Sperm competition and sperm phenotype[END_REF][START_REF] Parker | The evolution of expenditure on testes[END_REF]. In line with these predictions, it has been repeatedly observed that the production of larger ejaculates is indeed often associated with a higher fertilization success (e.g. Gage & Morrow 2003;Boschetto et al. 2011). Unsurprisingly, sexual selection has thus promoted the evolution of larger testes [START_REF] Parker | The evolution of expenditure on testes[END_REF] as well as a higher proportion of sperm-producing tissue within it (e.g. [START_REF] Lüpold | Sperm competition selects beyond relative testes size in birds[END_REF]) and a faster rate of spermatogenesis [START_REF] Ramm | Sperm competition and sperm length influence the rate of mammalian spermatogenesis[END_REF], under intense levels of sperm competition (e.g. in promiscuous species). Indeed, the selective pressure of sperm competition likely shapes multiple aspects of spermatogenesis affecting sperm production rate, from the number and activity of spermatogonial stem cells, the degree and architecture of their expansion and their post-meiotic differentiation into highly specialised sperm cells (Ramm et al. 2014;Ramm & Schärer 2014).

An increase in the number of sperm allocated per ejaculate is only one of the multiple pathways boosting fertilization success. Several features of the sperm cell itself have evolved in response to intense levels of sperm competition [START_REF] Pizzari | Sperm competition and sperm phenotype[END_REF]Fitzpatrick & Lüpold 2014). Among these characteristics, the positive influence of sperm motility (i.e. proportion of motile sperm within an ejaculate) and of average within-ejaculate sperm velocity on male fertilizing ability has been repeatedly documented [START_REF] Snook | Sperm in competition: not playing by the numbers[END_REF][START_REF] Pizzari | Sperm competition and sperm phenotype[END_REF]). These effects are explained by the fact that faster sperm will often reach female's gametes quicker than slower sperm (see for example Gage et al. 2004;[START_REF] Gasparini | Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri[END_REF] for evidence in external and internal fertilizers, respectively). Comparative analyses performed across various taxa have revealed that sperm swimming velocity increases with sperm size (e.g. Fitzpatrick et al. 2009 in fishes;Tourmente et al. 2011 in mammals), highlighting that various structural aspects of sperm -especially flagellum or midpiece length/volume -modulate sperm velocity [START_REF] Cardullo | Metabolic regulation in mammalian sperm: mitochondrial volume determines sperm length and flagellar beat frequency[END_REF][START_REF] Pizzari | Sperm competition and sperm phenotype[END_REF]. In primates, males from species where females mate with multiple partners display midpieces with a larger volume (Anderson & Dixson 2002). As larger midpieces are associated with a greater mitochondrial loading supporting sperm motion [START_REF] Gu | Comparative analysis of mammalian sperm ultrastructure reveals relationships between sperm morphology, mitochondrial functions and motility[END_REF], this increased midpiece volume appears to be adaptive when females mate with several males within a given breeding attempt.

In the next sections, we consider the various pathways through which allocation to these sperm traits imposes costs on males that likely result in accelerated ageing in reproduction or survivorship.

Energetic costs of sperm production. One tenet of our current understanding of the evolution of ageing relies on the energetically-demanding aspect of reproductive allocation (Kirkwood 2017), which is typically the case when it comes to producing an ejaculate and to growing and maintaining an efficient reproductive machinery (Kenagy & Trombulak 1986). Although earlier studies assumed that sperm were particularly cheap to produce (see Dewsbury 2005), the influence of resource availability on sperm production has been demonstrated in a wide spectrum of organisms. For instance, in fallow deer (Dama dama), a species in which females mate with several males during a given reproductive attempt (Briefer et al. 2013), yearling males with a diet supplemented with protein and amino acids have larger testes, exhibit Sertoli cells -which play a key nutritional function during spermatogenesis -with higher workload capacities, higher concentrations of sperm within the epididymis and sperm with a longer midpiece than do non-supplemented yearling males [START_REF] Kotrba | High-energy diet enhances spermatogenic function and increases sperm midpiece length in fallow deer (Dama dama) yearlings[END_REF]. This positive effect of an enriched diet on sperm quantity and/or quality has also been repeatedly found in agronomy research (e.g. [START_REF] Zhao | The effect of dietary grape pomace supplementation on epididymal sperm quality and testicular antioxidant ability in ram lambs[END_REF]) and in invertebrates. In cockroaches (Nauphoeta cinerea), for example, the number of sperm found in the spermatophore delivered to females (but not sperm viability) increases with the intake of both proteins and carbohydrates [START_REF] Bunning | Protein and carbohydrate intake influence sperm number and fertility in male cockroaches, but not sperm viability[END_REF]. The same relationships are observed in the Argentine ant (Linepithema humile), where a protein restriction in the diet during the larval stage (i.e. when the whole stock of sperm is produced) impairs sperm production but does not decrease sperm viability [START_REF] Dávila | Protein restriction affects sperm number but not sperm viability in male ants[END_REF]. In this social insect, a stronger allocation of the decreased quantity of resources to sperm quality (i.e. sperm viability) might be adaptive as sperm can be stored for several years before fertilization in the female spermathecae. Overall, the production of high-quality ejaculates largely depends on male condition and the quantity of resources that individuals can allocate to the post-copulatory traits [START_REF] Perry | Condition-dependent ejaculate size and composition in a ladybird beetle[END_REF], although the condition-dependent nature of ejaculate traits likely vary across species (see [START_REF] Macartney | Effects of nutrient limitation on sperm and seminal fluid: a systematic review and meta-analysis[END_REF] for a meta-analysis).

Limitations on resource availability that generally occur in the wild lead to an increase in the physiological costs of spermatogenesis. This is well illustrated in adders (Vipera berus), where the magnitude of testis growth prior to the reproductive season is positively correlated with body mass loss [START_REF] Olsson | Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus[END_REF]. In this species, the allocation to spermatogenesis (i.e. post-copulatory traits) accounts for a higher proportion of mass loss than the allocation to mate searching (i.e. pre-copulatory traits) [START_REF] Olsson | Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus[END_REF], which strongly suggests that the long-term ageing costs of mass loss generated by repeated reproductive seasons throughout life might not be trivial. It thus appears that males substantially allocating to sperm competition might -following the life history of ageing framework (Lemaître et al. 2015; Kirkwood 2017) -suffer from strong physiological costs (e.g. immune costs, as discussed in the next section) that will ultimately lead to a shorter lifespan and/or more pronounced ageing in fitness components.

Immune costs of sperm production. Pathogen-infected males generally have less efficient post-copulatory traits than uninfected males, whether pathogens are directly located in the ejaculate component (e.g. [START_REF] Cunningham | Male genital tract chlamydial infection: implications for pathology and infertility[END_REF] or not (e.g. [START_REF] Polak | Effects of ectoparasitism on host condition in the Drosophila-Macrocheles system[END_REF]. The negative association between the allocation to ejaculate-related traits and the performance of the immune system (or vice-versa) likely accounts for this difference (see Table 2 for a synthesis). For instance, in Arctic charr (Salvelinus alpinus) males, the density of granulocytes (i.e. white blood cells belonging to the non-specific immune system) is negatively correlated with the concentration of sperm within semen [START_REF] Liljedal | Secondary sex traits, parasites, immunity and ejaculate quality in the Arctic charr[END_REF].

Overall, the trade-off between ejaculate quality and immune performance is pervasive, even if a thorough investigation of the immune repertoire is required because the allocation to ejaculate-related traits might be negatively related to some immune cells while being positively associated with others (see [START_REF] Simmons | Bacterial immunity traded for sperm viability in male crickets[END_REF] for a case study in crickets, Teleogryllus oceanicus). This decreased activity of the immune system following an increased sperm production is adaptive because it minimizes the risk of autoimmunity, since antigens at the surface of sperm cells lead them to be recognized as foreign bodies by the immune cells (see [START_REF] Skau | Does immunity regulate ejaculate quality and fertility in humans[END_REF]. In line with this functional link, experimental evolution work in yellow dung flies (Scathophaga stercoraria) revealed that males from lines selected under an elevated sperm competition regime show lower phenoloxydase activity than males from monandrous lines [START_REF] Hosken | Sex and death: microevolutionary trade-offs between reproductive and immune investment in dung flies[END_REF], which makes these males more likely to suffer from an infection [START_REF] Mckean | Increased sexual activity reduces male immune function in Drosophila melanogaster[END_REF]. In addition, the negative association between sperm production and immunity might be directly reinforced by a resource-based allocation trade-off. This is well-illustrated in crickets (T. oceanicus), where the trade-off between antibacterial activity and sperm viability is only observed in individuals fed with a nutrientrestricted diet [START_REF] Simmons | Resource allocation trade-off between sperm quality and immunity in the field cricket, Teleogryllus oceanicus[END_REF].

Similar to what has already been reported for the allocation to growth and/or reproduction in males, or the male allocation to the growth and maintenance of pre-copulatory traits in males (Folstad & Karter 1992;[START_REF] Rödel | Reproductive effort alters immune parameters measured post-partum in European rabbits under semi-natural conditions[END_REF], a strong allocation to postcopulatory traits can be highly detrimental for male's immune performance (Table 2). As immunity constitutes a key physiological function mediating trade-offs among life-history traits [START_REF] Sheldon | Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology[END_REF], an elevated allocation to post-copulatory competition should have long-term consequences in terms of reduced lifespan and increased ageing rates through the impairment of immune performance throughout life.

Reproductive senescence costs of sperm production. Similar to what is observed for the allocation of resources to pre-copulatory traits in early life (Table 1), the long-term fitness costs of a strong allocation to sperm production could also be expressed in terms of reproductive ageing. Thus, in Drosophila melanogaster, an increased reproductive effort early in life has a negative impact on subsequent fertility, which is mediated by a pronounced agespecific decline in sperm numbers [START_REF] Prowse | The effects of reproduction on longevity and fertility in male Drosophila melanogaster[END_REF]. Similarly, in the domestic fowl (Gallus gallus domesticus), males that produce the highest quality sperm (judged through sperm velocity) during early life show the steepest decline in sperm quality in late life [START_REF] Cornwallis | Sex-specific patterns of aging in sexual ornaments and gametes[END_REF]. This suggests that males allocating a lot to the production of highquality ejaculates during early life might suffer from a stronger decline in reproductive success at late ages. Evidence that males naturally suffer from a decline in reproductive success with increasing age is widespread across the tree of life (Johnson & Gemmell 2012; First, the accumulation of mutations on the male germline throughout life (e.g. [START_REF] Velando | Senescent males carry premutagenic lesions in sperm[END_REF]Kong et al. 2012) might play a key role in causing reproductive ageing [START_REF] Monaghan | The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness[END_REF]. In that context, is selection for a higher allocation to sperm competition responsible for an increased mutation rate? And do elevated mating rates amplify this mutation load, as males need to replenish their sperm storage quickly to avoid sperm limitation (Dewsbury 1982;[START_REF] Nakatsuru | Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces, Characidae)[END_REF]? There is good evidence that high mating rates impair ejaculate quality in the short-run (e.g. [START_REF] Wedell | Male age, mating status and nuptial gift quality in a bushcricket[END_REF]) but whether the repeated and/or sustained activation of the spermatogenesis machinery influences fitness-related traits in late life is much less clear [START_REF] Vega-Trejo | The effects of male age, sperm age and mating history on ejaculate senescence[END_REF], as are the underlying mechanisms (Fricke & Koppik 2019). The degree to which mutations impact stem, transit or sperm cells themselves during spermatogenesis will be key to the long-term consequences of sperm allocation, and this in turn will partly depend on the hierarchical organisation of cell division within the testis, i.e. on its tissue architecture, which varies widely among species (see [START_REF] Schärer | Evolution of testicular architecture in the Drosophilidae: a role for sperm length[END_REF]Ramm & Schärer 2014). But as testicular stem cell activity increases to support greater sperm production under sperm competition, the burden of mutation and its manifestation in terms of reproductive ageing is predicted to increase (Blumenstiel 2007). To date, little work has been done to measure inter-and intraspecific variation in relevant parameters in response to sperm competition levels, but we know that in the flatworm Macrostomum lignano, an increased stem cell activity and corresponding faster speed of spermatogenesis support the enhanced sperm production that is selected when sperm competition occurs [START_REF] Schärer | Bigger testes do work more: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp[END_REF][START_REF] Giannakara | Sperm competition-induced plasticity in the speed of spermatogenesis[END_REF].

Moreover, recent evidence in seed beetles, Callosobruchus maculatus, suggests that the higher level of sperm production under sperm competition directly compromises the ability of the testis to maintain germline integrity, resulting in increased mutation loads being passed to offspring (Baur & Berger 2020).

Second, a plausible route linking sperm production to reproductive ageing is that increased gonadal activity might have direct detrimental consequences on male reproductive traits through an increased production of reactive oxygen species (ROS) [START_REF] Reinhardt | Evolutionary consequences of sperm cell aging[END_REF] Monaghan & Metcalfe 2019) -a factor known to influence ageing patterns (Finkel & Holbrook 2000). Thus, in rats, Rattus norvegicus, an increased sexual activity directly leads to an elevated level of oxidative stress within the testis [START_REF] Salomon | Oxidative stress in testis of animals during aging with and without reproductive activity[END_REF]. While repeatedly increased level of oxidative stress might cause impaired testicular function and sperm fertilization efficiency over time [START_REF] Aitken | Oxidative stress, sperm survival and fertility control[END_REF], and thereby increase reproductive ageing, empirical studies investigating this topic are currently lacking.

A third consideration regarding long-term consequences of increased sperm production concerns the fact that sperm competition has likely selected for the overexpression of genes promoting cell proliferation, notably in the spermatogonia (Kleene 2005; [START_REF] Lewis | Sperm competition, immunity, selfish genes and cancer[END_REF].

While the expression of such genes might convey an important competitive advantage in terms of ejaculate size and number, they are likely also to increase the risk of developing testicular cancer (see Kleene 2005; [START_REF] Lewis | Sperm competition, immunity, selfish genes and cancer[END_REF] for reviews), which could badly impair reproductive success in late life [START_REF] Huddart | Fertility, gonadal and sexual function in survivors of testicular cancer[END_REF]. So far, these relationships have been almost solely investigated in Drosophila spp. [START_REF] Hime | Drosophila spermatogenesis: insights into testicular cancer[END_REF], even though several studies are now documenting cancers across very diverse species (see [START_REF] Madsen | Cancer prevalence and etiology in wild and captive animals[END_REF][START_REF] Albuquerque | From humans to hydra: patterns of cancer across the tree of life[END_REF]. However, whether selection for enhanced sperm production under sperm competition is associated with an increased risk of getting cancer (and most specifically testicular cancer) at both intra-or inter-specific level is yet to be determined [START_REF] Lewis | Sperm competition, immunity, selfish genes and cancer[END_REF].

Finally, the maintenance of accurate and efficient physiological and cellular processes throughout life is fundamental to our current understanding of ageing (Kirkwood 2017;

Maklakov & Chapman 2019). In most animals, males have to allocate a substantial quantity of resources to mechanisms involved in the maintenance of the genome and proteome of the pool of germline stem cells [START_REF] Maklakov | The expensive germline and the evolution of ageing[END_REF]), and we expect that these costs should scale with sperm production capacity. These costs are probably far from negligible, since in laboratory mice the activity of enzymes repairing DNA is much greater in germ cells than in somatic cells (Intano et al. 2001). Moreover, among somatic cells, the enzymatic activity is higher in Sertoli cells than in those from other tissues (e.g. liver, brain), highlighting again the substantial maintenance costs associated with the male reproductive machinery (Intano et al.

2001

). With increasing age, males suffer from an age-specific decline in germline maintenance [START_REF] Maklakov | The expensive germline and the evolution of ageing[END_REF]), which might be responsible for an increased mutation rate on sperm in old males. However, whether the quantity of resources devoted to sperm competition limits the allocation to germline maintenance throughout life and ultimately triggers accelerated reproductive ageing remains to be investigated (but see Baur & Berger (2020) for a notable case study and [START_REF] Chen | Trade-off between somatic and germline repair in a vertebrate supports the expensive germ line hypothesis[END_REF] for experimental evidence that preventing allocation to the germline results in an enhanced ability for somatic repair).

Overall, although there are several well understood aspects of male reproductive ageing, the extent to which a strong resource allocation to traits shaping sperm competition in early life amplifies ageing and thus exacerbates the widely observed decrease of the male gonadal size and function with increasing age [START_REF] Lemaître | Reproductive senescence: new perspectives in the wild: Reproductive senescence in the wild[END_REF]Fricke & Koppik 2019;[START_REF] Santiago | Testicular aging: an overview of ultrastructural, cellular, and molecular alterations[END_REF]) remains an open question. Answering it is of crucial importance, since such effects might not only reinforce male reproductive ageing (e.g. through a decrease in sperm quantity) but could also lead to deleterious consequences more generally for male condition and health (Bribiescas 2006) -for example, through a decline in testosterone production over the life course (see Yeap 2009) -which could ultimately impact lifespan and survival ageing patterns (Bribiescas 2006, see next section). These interactions between ageing in reproduction and survivorship might be even more complex as organisms have to partition a limited resource pool between germline and somatic maintenance (Figure 1; [START_REF] Maklakov | The expensive germline and the evolution of ageing[END_REF]) and selection to maintain the integrity of the germline might be particularly strong (Kirkwood 2005;[START_REF] Maklakov | The expensive germline and the evolution of ageing[END_REF]. Hence, maintaining germline integrity under sperm competition likely gets harder (as so many more sperm need to be produced), and this may lead somatic maintenance (see [START_REF] Chen | Trade-off between somatic and germline repair in a vertebrate supports the expensive germ line hypothesis[END_REF] for recent evidence in vertebrates) and ultimately lifespan to be traded against sperm competition to get immediate benefits in terms of reproductive output.

Lifespan and survival ageing costs of sperm production. Despite the accumulation of evidence that a strong allocation to sperm production can entail acute physiological costs, its long-term consequences in terms of lifespan or survival ageing have been largely overlooked.

Yet, some studies performed on insects have revealed that high mating rates can shorten male lifespan [START_REF] Partridge | Sexual activity reduces lifespan of male fruitflies[END_REF][START_REF] Martin | Copulation reduces male but not female longevity in Saltella sphondylli (Diptera: Sepsidae)[END_REF][START_REF] Paukku | Cost of reproduction in Callosobruchus maculatus: effects of mating on male longevity and the effect of male mating status on female longevity[END_REF][START_REF] Dao | Reproduction-longevity trade-off in Anopheles gambiae (Diptera: Culicidae)[END_REF][START_REF] Metzler | Mating and longevity in ant males[END_REF]Jehan et al. 2020), which might be due to the downregulation of the expression of some specific genes (e.g. metabolic genes) straight after sexual activity (Branco et al. 2017). However, although sperm competition and mating rate are often related [START_REF] Parker | Sperm competition, mating rate and the evolution of testis and ejaculate sizes: a population model[END_REF], mating rate depends also on the number of receptive females in the population rather than purely the number of competing males, and so a high mating rate alone does not constitute the most accurate proxy of a strong resource allocation to sperm competition [START_REF] Vahed | The evolution of large testes: sperm competition or male mating rate[END_REF]. The relative influence of sperm production and mating rate per se on lifespan was disentangled in a pioneering experiment carried out on Caenorhabditis elegans (Van Voorhies 1992). Males (and hermaphrodites) carrying a mutant spe-26 gene showed a reduced rate of sperm production but a 65% increased lifespan compared to wild-type worms, but this gain was not amplified when mutant males were prevented from mating, suggesting that the long-term fitness costs strictly associated with sperm production are far from negligible (Van Voorhies 1992). Despite these promising results, the survival costs of sperm production have remained largely understudied. Yet, in large milkweed bug (Oncopeltus fasciatus), males fed with an ancestral seed diet show a higher sperm production at the expense of a reduced lifespan (Duxbury et al. 2018).

Moreover, in domestic fowl (Gallus gallus domesticus), males that produce the highest quantity of sperm through life show a reduced lifespan [START_REF] Cornwallis | Sex-specific patterns of aging in sexual ornaments and gametes[END_REF] while in the guppy (Poecilia reticulata), the opposite pattern occurs [START_REF] Gasparini | Sexual selection and ageing: interplay between pre-and post-copulatory traits senescence in the guppy[END_REF]).

We thus emphasize that studies at the interplay of sexual selection and ageing should now seek to accurately quantify these long-term survival costs (Figure 1), which would strongly contribute to understanding the diversity of life history strategies observed across the tree of life. Importantly, such studies should investigate whether the survival costs of an increased allocation to sperm competition is mediated by an acceleration of ageing rather than an immediate rise of the risk of death [START_REF] Partridge | The effect of reproductive activity on the longevity of male Drosophila melanogaster is not caused by an acceleration of ageing[END_REF]. The phylogeneticallycontrolled comparison of male actuarial senescence patterns across species displaying contrasted mating systems or -more accurately -a high variation in the rate of multiple paternity (e.g. Soulsbury 2010 in mammals) would provide complementary insights on the role played by sperm competition in shaping lifespan and actuarial senescence patterns in males. In addition, analyses performed at the population level will enable tests of whether these long-term survival costs are a consequence of an earlier age at the onset of ageing, an increased rate of ageing, or both [START_REF] Péron | Variation in actuarial senescence does not reflect life span variation across mammals[END_REF].

(b) Seminal fluid

Male fertilization success is also modulated by the non-sperm components of the ejaculate [START_REF] Perry | The seminal symphony: how to compose an ejaculate[END_REF], with comparative (e.g. [START_REF] Ramm | Sperm competition and the evolution of male reproductive anatomy in rodents[END_REF] and experimental (e.g. [START_REF] Simmons | Sexual Selection Shapes Seminal Vesicle Secretion Gene Expression in House Mice[END_REF]) data pointing towards the importance of increased allocation to seminal fluid under heightened levels of sperm competition. Interestingly, the female ageing cost of repeated exposure to male seminal fluid content has been studied extensively (see box 1). By contrast, whether the selection acting on the production of complex seminal fluid is associated with long-term ageing costs in males has largely been overlooked.

Multiple lines of evidence suggest that seminal fluid production is energetically costly (see also Table 2). Metabolic labelling studies in mice indicate that seminal fluid-producing tissues exhibit high rates of protein turnover [START_REF] Claydon | Heterogenous turnover of sperm and seminal vesicle proteins in the mouse revealed by dynamic metabolic labeling[END_REF]. In some taxa, seminal fluid allocation can reach extreme proportions. This is well illustrated in several species of bushcrickets where a single water-and protein-rich spermatophore transferred to a female can represent as much as 40% of male body mass [START_REF] Vahed | Larger ejaculate volumes are associated with a lower degree of polyandry across bushcricket taxa[END_REF]), but also in butterflies where the production of the sphragis (i.e. an external plug secreted by the male accessory glands and fixed to the female abdomen to impair further the access to the female genitalia) by males can constitute up to 20% of the male body mass [START_REF] Carvalho | A review of the occurrence and diversity of the sphragis in butterflies (Lepidoptera, Papilionoidea)[END_REF]. In line with these observations, a recent meta-analysis highlighted that the production of seminal fluid show a higher degree of condition-dependence than sperm production per se [START_REF] Macartney | Effects of nutrient limitation on sperm and seminal fluid: a systematic review and meta-analysis[END_REF].

Moreover, studies of accessory gland size in Drosophila, bedbugs and snails all suggest that seminal fluid production may limit male mating rate [START_REF] De Boer | Nervous control of male sexual drive in the hermaphroditic snail Lymnaea stagnalis[END_REF]Bangham et al. 2002;[START_REF] Reinhardt | Male mating rate is constrained by seminal fluid availability in bedbugs, Cimex lectularius[END_REF], implying that replenishment of seminal fluid protein reserves after mating is a non-trivial cost to males. Finally, while the male competitive advantage of producing large amounts of seminal fluid as well as the deleterious consequences for females (see Box 1) have been well described in the literature (e.g. [START_REF] Wigby | Seminal fluid protein allocation and male reproductive success[END_REF], the potential toxic effects and associated ageing consequences to their repeated storage in male's gonad are yet to be investigated.

Because males usually produce both sperm and seminal fluid simultaneously, however, it is difficult to tease apart the relative costs of these two ejaculate components. This difficulty is circumvented in red-sided garter snakes, Thamnophis sirtalis parietalis, in which spermatogenesis and seminal fluid (copulatory plug) production occurs at different times of the year. Whilst sperm are produced in the late summer and then stored over-winter, seminal fluid production does not occur until the onset of the mating (and fasting) season in spring.

Friesen and colleagues (2015) took advantage of these biological features to establish that the elevated metabolic rate associated with plug production are considerable, comparable even to those incurred by pregnant females. They further showed that these costs are especially pronounced in small males and, importantly, were able to quantify the energetic costs of producing a single copulatory plug (up to 18% of the daily energy expenditure). Their estimate reinforces earlier evidence of substantial mating costs based on the heightened blood lactate levels observed in mating vs. only courting males [START_REF] Shine | Mechanisms and consequences of sexual conflict in garter snakes (Thamnophis sirtalis, Colubridae)[END_REF]). These high energetic costs mean males can only deposit 1-2 plugs per day (Friesen et al. 2013) and again clearly challenge the traditional idea that seminal fluid production is a trivial expense to males. Whether the substantial costs of seminal fluid production translate into increased ageing is currently unclear, due simply to a paucity of relevant data. However, Koppik and colleagues (2018) recently discovered that, at old ages, sexually active male D. melanogaster display shorter mating, resulting in a lower number of eggs laid by females than following mating with virgin males. However, this pattern might be more likely due to a decrease in sperm number rather than in the quantity of seminal fluid proteins delivered to females, when sexually active males are reaching old ages (see [START_REF] Sepil | Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila[END_REF].

MITIGATION OF THE AGEING COSTS OF SPERM COMPETITION IN THE

WILD

The evidence compiled above suggests that a strong allocation to traits associated with an advantage when sperm competition occurs may be associated with some underestimated fitness costs, such as a shortened lifespan or increased ageing. One might thus expect that counter-adaptations have evolved to buffer the cascade of physiological costs and their fitness consequences. We discuss below some of these possible adaptations and evaluate how much they can mitigate fitness costs.

(a) Phenotypic plasticity in ejaculate production

Within species, sperm competition levels can fluctuate considerably across reproductive seasons and among populations. One way to minimize the various physiological costs potentially associated with elevated ejaculate expenditure would be to adjust ejaculate quality and quantity to the level of sperm competition. Such fine-scale adjustments require the evolution of phenotypic plasticity in the male reproductive machinery. Experimental manipulations of the social environment faced during the developmental period reveal that such plasticity might be common. For instance, in house mice (Mus musculus) males that were repeatedly in contact with the odour of multiple unrelated (i.e. rival) males had an elevated sperm production rate compared to males that were in contact to the odour of only a single competitor [START_REF] Ramm | Adaptive plasticity of mammalian sperm production in response to social experience[END_REF]. A similar experimental design revealed that in bank voles (Myodes glareolus), males who developed under environmental conditions mimicking high levels of sperm competition developed larger seminal vesicles (but similar testis mass) than males who developed under environmental conditions mimicking low levels of sperm competition [START_REF] Lemaitre | Social cues of sperm competition influence accessory reproductive gland size in a promiscuous mammal[END_REF]. Overall, this suggests that the allocation to postcopulatory traits is modulated in response to (social) environmental conditions, a characteristic that is widely shared across animal species for various sperm and non-sperm ejaculate traits (e.g. Immler et al. 2010 in birds;[START_REF] Stockley | Plasticity in reproductive effort of male dung flies (Scatophaga stercoraria) as a response to larval density[END_REF][START_REF] Simmons | Socially cued seminal fluid gene expression mediates responses in ejaculate quality to sperm competition risk[END_REF]Sloan et al. 2018 in insects;Nakadera et al. 2019 in snails;Janicke et al. 2013;[START_REF] Giannakara | Sperm competition-induced plasticity in the speed of spermatogenesis[END_REF][START_REF] Ramm | Sex allocation plasticity on a transcriptome scale: Socially sensitive gene expression in a simultaneous hermaphrodite[END_REF] in flatworms; [START_REF] Tan | Social group size, potential sperm competition and reproductive investment in a hermaphroditic leech, Helobdella papillornata (Euhirudinea: Glossiphoniidae)[END_REF]

in leeches and

Crean & Marshall 2008 in a broadcast spawning ascidian). Such fine-tuning to match the prevailing demand -or in other words, minimizing the expenditure where possible -may thus be one of the means through which males can limit the substantial physiological costs associated with the high metabolic demand of spermatogenesis and seminal fluid production.

In line with this prediction, an experiment performed in D. melanogaster has revealed that males reared with rivals produced more offspring during early life (in non-competitive trials) but paid a long-term survival cost with a median lifespan reduced by 19% (Bretman et al. 2013), which suggests that curtailing ejaculate production in absence of competitors might limit long-term ageing costs.

(b) Context-dependent sperm allocation

In addition to fine-tuning how many resources to expend on ejaculate production, a further level of male allocation likely occurs with respect to how many sperm and/or how much seminal fluid is transferred in each individual ejaculate. Thus, whilst traditionally assumed to be cheap, it has now been recognised for some time that males should prudently allocate ejaculate components according to relevant cues of sperm competition at the time of mating (see [START_REF] Wedell | Sperm competition, male prudence and sperm-limited females[END_REF][START_REF] Cameron | Sperm competition and the evolution of ejaculate composition[END_REF][START_REF] Parker | Sperm competition and ejaculate economics[END_REF]Perry et al. 2013 for reviews). For example, it typically pays to allocate more sperm per ejaculate under conditions of high sperm competition risk (e.g. [START_REF] Delbarco-Trillo | Male mammals respond to a risk of sperm competition conveyed by odours of conspecific males[END_REF], to allocate fewer per ejaculate at high sperm competition intensity (e.g. [START_REF] Pilastro | Individual adjustment of sperm expenditure accords with sperm competition theory[END_REF], to adjust the proteins compounds of the seminal fluid according to the degree of sperm competition [START_REF] Hopkins | Divergent allocation of sperm and the seminal proteome along a competition gradient in Drosophila melanogaster[END_REF] and to modulate ejaculate size depending on own social status (e.g. Bartlett et al. 2017) or to the male mating order and female reproductive status [START_REF] Thomas | Male crickets adjust the viability of their sperm in response to female mating status[END_REF].

Whilst these responses can be understood in terms of maximising fitness returns given a certain gamete number (or seminal fluid amount) available to allocate, they ultimately stem from the fact that the ejaculate supply is limited -one reason for which being that producing both sperm and non-sperm ejaculate components likely imposes substantial costs, many of which may ultimately increase the intensity of ageing.

(c) Sperm production seasonality

Besides using cues from their social environment to fine-tune sperm production and allocation, males of many taxa also show clear seasonal variation in traits such as testis size and sperm in storage, with peak production or availability often timed to coincide with a specific breeding season (reviewed in Ramm & Schärer 2014). In male fallow deer, for example, there is a three-fold increase in testis volume from its minimum to its peak just before the annual rut [START_REF] Gosch | Seasonal changes of testis volume and sperm quality in adult fallow deer (Dama dama) and their relationship to the antler cycle[END_REF]; for a broader survey across mammals, see [START_REF] Setchell | Anatomy, vasculature, and innervation of the male reproductive tract[END_REF]. Even more marked variation is reported in other taxa with highly seasonal reproductive seasons such as the annual variation observed in male (and female) gonado-somatic index in many broadcast spawners (see Parker et al. 2018 and references therein) and some fishes (e.g. [START_REF] Turner | The seasonal cycle in the spermary of the perch[END_REF]. As discussed by Ramm and Schärer (2014), such seasonal variation can be accompanied by specific features of spermatogenesis, such as the long branch lengths (many rounds of mitotic division) observed for example in cichlids, meaning thousands of spermatids are produced per primary spermatogonium, supporting the delivery of a large number of sperm at a specific time of the year (Fishelson 2003). These and other features emphasize the expensive nature of spermatogenesis. Moreover, as we have seen, the fact that sperm production sometimes occurs asynchronously with the breeding season -when energetic demand from other traits such as mate searching, pre-copulatory competition and courtship also peaks -is probably also indicative of its high costs [START_REF] Olsson | Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus[END_REF]. However, we cannot rule out that in some species, such uncoupling might be a constraint associated with prolonged periods of torpor [START_REF] Gustafson | Male reproductive patterns in hibernating bats[END_REF].

Overall, we expect that the 'savings' to be made from seasonal fluctuation in ejaculate production will be highly species-specific and depend on its particular reproductive ecology, but that matching supply and demand in this manner is a widespread mechanism to minimise the energetic and other costs outlined above, all of which would otherwise ultimately feedback on accelerated survival and/or reproductive ageing.

ROADMAP FOR FUTURE RESEARCH

Overall, studies that seek to quantify the long-term ageing cost of a strong allocation to sperm competition and to decipher the underlying physiological pathways are thus badly required.

Such studies would undeniably enhance our knowledge in two main areas of evolutionary ecology, namely sexual selection and ageing. We propose below a few potential avenues for future research.

(a) Do production plasticity, resource allocation and seasonality limit male ageing?

Whilst at some level it is clear that any reduction in ejaculate demand must ultimately be less costly than the alternative, few studies have to date sought to use either intra-or interspecific variation in, for example, the incidence of sperm competition or length of the breeding season to better understand the nature and magnitude of these costs, or to quantify their impact on ageing of fitness components. Comparative work in this area is likely to be highly informative, and one of the most promising of all would be experimental approaches that seek to modify one or more of these axes and then measure the ageing consequences. Potentially useful approaches here might include experimental evolution to test for the correlated evolution of ageing effects in lines selected for higher or lower allocation toward sperm competition traits or under different intensity of sexual conflict. Recent experiments performed in D. melanogaster have revealed that males from monogamous lines (i.e. without sperm competition) reduce their allocation to various post-copulatory traits. For instance, they show a lower expression of genes coding for seminal fluid proteins compared to males from polygamous lines [START_REF] Hollis | Sexual conflict drives male manipulation of female postmating responses in Drosophila melanogaster[END_REF]. Investigating whether these males also display a delayed and/or reduced reproductive and/or survival senescence patterns compared to males evolving under competitive conditions would be very informative to assess whether natural and sexual selection have fine-tuned the allocation to post-copulatory traits to limit its detrimental ageing consequences.

Where experimentally feasible, the direct manipulation of relevant physiological pathways involved in ejaculate production using gene knockdown or gene-editing techniques would also be insightful. By thereby manipulating the capacity for plasticity or allocation, one could more precisely identify the mechanisms involved in both short-and long-term fitness consequences. Precisely such an approach was recently adopted to test for a trade-off between germline and somatic maintenance in the zebrafish Danio rerio [START_REF] Chen | Trade-off between somatic and germline repair in a vertebrate supports the expensive germ line hypothesis[END_REF]. Unmanipulated and germline-free knockdown individuals were exposed to sublethal low-dose ionizing radiation, revealing that somatic recovery occurred much faster in the germline-free individuals that were prevented from allocating to reproduction [START_REF] Chen | Trade-off between somatic and germline repair in a vertebrate supports the expensive germ line hypothesis[END_REF]. These results thus support the idea that germline maintenance is costly. As we emphasized above, these costs likely scale with sperm competition level. Finally, experimental manipulations of the quantity of resources available in the environment would also provide relevant insights.

As emphasized above, the allocation to ejaculate production increases with resource availability [START_REF] Zhao | The effect of dietary grape pomace supplementation on epididymal sperm quality and testicular antioxidant ability in ram lambs[END_REF][START_REF] Kotrba | High-energy diet enhances spermatogenic function and increases sperm midpiece length in fallow deer (Dama dama) yearlings[END_REF]. Therefore, for a given level of sperm competition perceived in the environment, we can predict that males should their increase their allocation to post-copulatory competition, at no or very limited costs in terms of ageing.

(b) Ageing consequences of allocation to both pre-and post-copulatory traits in a trade-off world

As pointed out in the Introduction, male allocation to sexual competition is a complex process encompassing both a pre-and post-copulatory phase [START_REF] Parker | Sperm competition and the evolution of ejaculates: towards a theory base[END_REF]). While we have demonstrated in this perspective article that allocation to post-copulatory competition is likely to be associated with long-term ageing costs, substantial evidence that the competition for gaining mating opportunities also shortens lifespan and accelerates ageing in terms of both reproduction and survival has accumulated (e.g. Bonduriansky et al. 2008; Table 1). The physiological pathways involved in mediating the relationships between the allocation to preor post-copulatory competition on the one hand and those linking them to ageing on the other are also likely to strongly overlap. For instance, in three-spined sticklebacks (Gasterosteus aculeatus), males with an increased carotenoid-based red coloration on their cheeks and throats show the strongest levels of oxidative DNA damage in both sperm and somatic tissues (Kim & Velando 2020), which highlights that a resource-based allocation trade-off between sexual selection and somatic maintenance mediates the long-term ageing costs of both preand post-copulatory sexual competition. Interestingly, as allocation to both primary (e.g. sperm-producing tissue within the testes) and secondary (e.g. ornaments and armaments) sexually-selected traits relies on the quantity of resources available in the environment, males cannot maximize both aspects of allocation to sexual competition simultaneously [START_REF] Parker | Sperm competition and the evolution of ejaculates: towards a theory base[END_REF][START_REF] Parker | Sperm competition games: a general model for precopulatory male-male competition[END_REF]. Evidence for trade-offs between pre-and post-copulatory traits are widespread in nature, at both inter-and intra-specific levels (see Simmons et al. 2017 for a review). For instance, across pinnipeds, the relative testes mass and the degree of sexual size dimorphism are negatively correlated (Fitzpatrick et al. 2012). Overall, the resourceallocation strategy towards pre-and post-copulatory competition is likely fine-tuned by the fitness payoff of favoring one set of sexual traits at the expense of the other, which is likely to result from complex interactions between species-or population-specific traits (e.g. mating system, mating tactic) (Simmons et al. 2017) and environmental characteristics determining the nature and degree of sexual competition [START_REF] Vahed | The evolution of large testes: sperm competition or male mating rate[END_REF]. In practice, it is particularly difficult to predict what aspects of sexual competition will predominantly drive the physiological costs of sexual selection (e.g. [START_REF] Olsson | Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus[END_REF] in the case of adders), especially since the relative allocation to each sexual trait might change over the male's life course [START_REF] Lemaître | Reproductive senescence: new perspectives in the wild: Reproductive senescence in the wild[END_REF]. Nevertheless, any thorough investigation of the ageing costs of sexual selection should consider the cumulative costs associated with both aspects of a male's allocation to sexual competition, which is lacking to date.

(c) Contribution to the sex differences in lifespan and ageing across species

In most species, males and females differ in lifespan and ageing patterns (Austad 2011;Austad & Fischer 2016;[START_REF] Marais | Sex-specific differences in aging and longevity: can sex chromosomes play a role?[END_REF]. While some factors (e.g. sex chromosomes) provide relevant explanations for the average direction in sex differences in lifespan across species [START_REF] Xirocostas | The sex with the reduced sex chromosome dies earlier: a comparison across the tree of life[END_REF], the evolutionary roots of the large magnitude of sex differences in lifespan and ageing patterns observed across species remain poorly understood (see Lemaître et al. 2020 in mammals). So far, most comparative analyses that seek to explain this diversity have focused on the role of sexual selection (e.g. [START_REF] Clutton-Brock | Sex differences in ageing in natural populations of vertebrates[END_REF], with the expectation that sex differences in lifespan and ageing rates should increase in species where males devote a substantial amount of resources to pre-copulatory competition (generally measured through the degree of sexual size dimorphism, see [START_REF] Tidière | Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants[END_REF].

However, these results remain largely equivocal and current evidence that the allocation to pre-copulatory competition influences the evolution of sex differences in lifespan and ageing in wild populations is limited at best [START_REF] Lemaître | Sex differences in adult lifespan and aging rates of mortality across wild mammals[END_REF]. Here, we argue that comparative analyses should carefully consider the long-term costs associated with post-copulatory competition, which might also contribute to shaping the magnitude of sex differences in lifespan and ageing patterns. Species displaying high levels of sperm competition should allocate a much higher quantity of resources towards germline maintenance, at the expense of somatic maintenance [START_REF] Maklakov | The expensive germline and the evolution of ageing[END_REF]. So far, these long-term costs have only been considered in an analysis focused on large herbivores and in this study, species-specific allocation to post-copulatory competition -measured by the relative testes mass -did not influence the degree of sexual size dimorphism in lifespan (Lemaître & Gaillard 2013a).

However, the mean allocation to testis size is weak and shows little variation among large herbivores compared to other taxa [START_REF] Gomendio | Why mammalian lineages respond differently to sexual selection: metabolic rate constrains the evolution of sperm size[END_REF], and similar analyses need to be performed using a broader taxonomic range. Moreover, such studies should fully embrace the multi-dimensional nature of allocation to post-copulatory competition by considering not just relative testes mass but also several other costly sperm features (e.g. size, velocity) and the level of allocation to the seminal fluid component of the ejaculate. In addition, such interspecific studies should control for the basal metabolic rate, as species displaying a high massspecific metabolic rate can more easily allocate to high quality ejaculates (e.g. through the production of particularly long sperm, see [START_REF] Gomendio | Why mammalian lineages respond differently to sexual selection: metabolic rate constrains the evolution of sperm size[END_REF]. Lastly, such comparative analyses should include the socio-ecological context. As shown above, the environmental conditions that affect the amount of available food resources, the habitat heterogeneity that influences spatial distribution of both sexes and the level of sexual segregation, and the population size and structure that define the operational sex ratio and female group size distribution should all determine the male investment corresponding to a given allocation to traits that shape the intensity of post-copulatory competition, and thereby fine-tune this allocation (Figure 1). Species-specific differences in the level of sperm competition could also shape diverse patterns of reproductive ageing in males (and thus various patterns of sex differences in reproductive ageing). Interestingly, a comparative analysis performed across 18 species of rodents maintained in lab conditions revealed a positive relationship between levels of sperm competition and DNA fragmentation among sperm [START_REF] Delbarco-Trillo | A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation[END_REF], which suggests that inter-specific differences in the level of sperm competition can explain betweenspecies differences in sperm integrity. Whether these differences are exacerbated with increasing age and occur in the wild is unknown but this clearly deserves attention. Recently, delBarco-Trillo and colleagues (2018) compared different post-copulatory traits (e.g. relative testes mass, various sperm features) between a small sample of young and old males for three species of rodents, all belonging to the genus Mus and displaying contrasting levels of sperm competition. While this transversal study did not reveal any clear difference in the agespecific changes in post-copulatory traits among these three species, it clearly set out a promising framework for future longitudinal studies comparing the age-specific decline in post-copulatory traits over the life course of individuals and across a wider range of species.

The study of male reproductive ageing is currently attracting significant attention in evolutionary ecology [START_REF] Lemaître | Reproductive senescence: new perspectives in the wild: Reproductive senescence in the wild[END_REF]Fricke & Koppik 2019;[START_REF] Monaghan | The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness[END_REF] and such approaches would be particularly relevant to understand the evolutionary roots of male reproductive ageing. , 200, 941-951. Dewsbury, D.A. (1982). Ejaculate cost and male choice. The American Naturalist, 119, 601-610. Dewsbury, D.A. (2005) 2005), notably in late life. Among these adaptations, the role played by male seminal fluid proteins constitutes an iconic example.

Biology

Seminal fluid proteins can have various detrimental effects for females [START_REF] Poiani | Complexity of seminal fluid: a review[END_REF]) and those are particularly well studied in the fruit fly, D. melanogaster. In this species, the repeated exposure to seminal fluid proteins transferred during copulation increases female death rate [START_REF] Chapman | Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products[END_REF]. More specifically, the decrease in female survival prospects appears to be predominantly caused by the sex-peptide [START_REF] Wigby | Sex peptide causes mating costs in female Drosophila melanogaster[END_REF]) -a protein produced by the male accessory glands -that enhances male reproductive success in a competitive context by reducing the degree of female receptivity and increasing sperm storage by females [START_REF] Chapman | The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference[END_REF]Avila et al. 2010). The female-specific deleterious effects of male sex peptide on lifespan and late-life reproductive success are mediated by several physiological pathways, notably through a rise in the release of juvenile hormones (Edward & Chapman 2011). Strikingly, it has been recently shown that -independently of the transfer of sex peptide -both mating and the amount of exposure to males not only decrease female survival but also increase the degree of physiological ageing (measured by the age-specific decline in climbing activity and starvation resistance) (Bretman & Fricke 2019). These results strongly emphasize the complexity of the interactions between mating rates, physiological processes and both reproductive and survival ageing in females.

While the production of seminal fluid proteins in response to sperm competition and its consequence for female's ageing are well studied -at least in flies -studying other instances of sexual conflict over mating and fertilization might shed interesting light on the evolution of demographic ageing in females. This is well illustrated by the very peculiar genitalia that have evolved to improve sperm transfer abilities, and more generally, fertilization efficiency in many species (Eberhard 1985) and that are already known to influence female survival in the short run (e.g. [START_REF] Crudgington | Genital damage, kicking and early death[END_REF]. Across mammals, the level of polyandry (measured by the species-specific relative testes mass) does not seem to increase the female rate of ageing in survivorship (Lemaître & Gaillard 2013b). However, keratinized spines found at the surface of the penis of several mammalian species (e.g. some primates, rodents and felids) can be responsible for lesions of the female reproductive tract [START_REF] Orr | All features great and small-the potential roles of the baculum and penile spines in mammals[END_REF], which could ultimately compromise the late-life reproductive success of the most polyandrous females.

Finally, high levels of polyandry are associated with a higher risk of contracting sexually transmitted diseases [START_REF] Thrall | Sexual transmission of disease and host mating systems: within-season reproductive success[END_REF]) that can impair reproductive success and survival in the long-run [START_REF] Sheldon | Sexually transmitted disease in birds: occurrence and evolutionary significance[END_REF]. To counteract these adverse effects, polyandrous females have evolved immune systems that might mitigate these fitness costs through an increased resistance to infections (e.g. Nunn et al. 2000 in primates). This is well illustrated in lizards (Zootoca vivipara) where polyandrous females show a greater ability to mount an inflammatory immune response than monandrous females [START_REF] Richard | Litter quality and inflammatory response are dependent on mating strategy in a reptile[END_REF]. While a greater allocation of resources to immune defences in polyandrous females is likely to convey fitness benefits at a short-time scale, they might also lead to an overall increased rate of ageing through an over-activation of the immune system (e.g. inflammaging) (Franceschi et al. 2000). Yet, how much this and many other consequences of male allocation to sperm competition contribute to the observed differences in female ageing at both inter-and intraspecific levels is yet to be determined.

Lemaître&

  Gaillard 2017), and the (epi)genetic and physiological mechanisms underlying this decline are diverse (Evans et al. 2019; Fricke & Koppik 2019; Monaghan & Metcalfe 2019). Here we discuss four related aspects that seem especially relevant when sperm competition occurs.

Table 1 :

 1 Evidence of long-term lifespan and ageing costs associated to an increased allocation to pre-copulatory competition. Such relationships have been assessed across different types of populations (L: laboratory, W: wild populations, SC: of the functional relationships linking the allocation of resources to sperm competition traits with increased ageing in both reproduction and survivorship (i.e. denoted by the shift from the black to the red trajectories on the ageing curves). While some environmental conditions (e.g. pollution) can directly increase the mutation load on both germline and somatic tissues, they also largely modulate the socioenvironmental context (e.g. adult sex ratio) that determines the level of sperm competition within a population. These ageing consequences are likely to be mediated by multiple physiological pathways leading to a progressive deterioration of the germline (e.g. through an accumulation of mutations on sperm DNA) and the soma (e.g. a decrease in the efficiency of the somatic gonad and an impairment of some key physiological functions such as immunity).

Sperm competition influences ageing in females

  . The Darwin-Bateman paradigm in historical context.Integrative and Comparative Biology, 45, 831-837. Duxbury, A.E., Weathersby, B., Sanchez, Z. & Moore, P.J. (2018). A study of the transit amplification divisions during spermatogenesis in Oncopetus fasciatus to assess plasticity in sperm numbers or sperm viability under different diets. In contrast to males, the consequences of sperm competition for female lifespan and ageing have been well studied. By aiming to answer the question "why do females mate with multiple males in most species?", behavioural ecologists have provided compelling evidence that polyandry (i.e. the female propensity to mate with several males and thus to incite sperm competition among males) is associated with both benefits and costs(Jennions & Petrie 2000). In males, sperm competition has led to the evolution of many behavioural, anatomical and physiological adaptations that increase the probability to fertilize a female's eggs(Birkhead & Møller 1998). However, several of these adaptations can have detrimental effects on female reproductive success and survival (reviewed in[START_REF] Stockley | Sexual conflict resulting from adaptations to sperm competition[END_REF] Arnqvist & Rowe

	Ecology and Eberhard, W.G. (1985). Sexual selection and animal genitalia. Harvard University Press evolution, 8, 10460-10469. Cambridge, MA. Edward, D.A. & Chapman, T. (2011). Mechanisms underlying costs of reproduction. Evans, J., Wilson, A., Pilastro, A. & Garcia-Gonzalez, F. (2019). Ejaculate-mediated paternal effects: evidence, mechanisms and evolutionary implications. Reproduction, 157,R109-R126. BOX 1:

The sperm allocation is used as a proxy of sperm production.

The activity of the phenoloxidase is reduced but there was no effect on the hemocyte load.

Damages found on proteins (carbonylation levels) but sexual activity of males shows an increase in anti-oxidant defences that could probably buffer oxidative costs.

ACKOWLEDGMENTS J. -F. L. and J. -M. G. were supported by a grant from the Agence Nationale de la Recherche (ANR-15-CE32-0002-01). This work was performed within the framework of the LABEX ECOFECT (ANR-11-LABX-0048) of Université de Lyon, within the program ''Investissements d'Avenir'' (ANR-11-IDEX-0007) operated by the French National

Research Agency (ANR). We are extremely thankful to Mathieu Douhard, Alexei Maklakov and Geoff Parker for insightful comments on earlier drafts of this work. We also thank three anonymous referees for insightful and constructive comments that markedly improved our manuscript.

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Insect

Fruit 1 Articles linking horn length (or horn growth) to lifespan in bovids were deliberately omitted because these studies have been subjected to some controversies, due to the possible confounding effects of trophy hunting (see Lemaître et al. 2018 for a compilation of these studies).

2 Reproductive senescence measured by the age-specific decline in calling activity.

3 Reproductive senescence measured by the age-specific decline in ejaculate quality. 4 Reproductive senescence measured by the age-specific decline in harem size.

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