Sex Differences in Parental Care

Sex differences in parental care

Hanna Kokko, Michael D Jennions

Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia

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6.1 Introduction

Have a look at the images in Fig. 6.1. Although you might not be able to identify the species, can you tell which individual is the male, and which is the female? If you always picked the animal on the left as the male you were correct. Why is it that we can often tell the sexes apart, even in a species we have never seen before?

In general, the assumption that females are the main care-givers is biologically justified. In about 90% of mammals, males inseminate females, fertilize eggs and thereafter provide no parental care. Likewise, in arthropods there is a very strong bias towards female-only parental care. Biparental care is rare, and male-only care has only evolved in eight of the many lineages in this enormous taxonomic group (Tallamy 2000) (although new discoveries of male-only care continue to be made; e.g. Requena et al. 2010). In reptiles parental care is uncommon: eggs are usual buried and abandoned. However, when egg guarding occurs it is almost always by the female, with biparental care having evolved from female-only care in some crocodilians (De Fraipont et al. 1996; Reynolds et al. 2002). In birds, the sex bias in parental care is weaker but still present. There is female-only care in 8% of species, biparental care in about 81% of species, and biparental care with input from helpers occurs in another 9% of cooperatively breeding species (Cockburn 2006). Even when both parents care there is, however, still a propensity for the female to spend more time building the nest and incubating eggs (Schwagmeyer et al. 1999; Møller & Cuervo 2000).

Before we become too confident in our abilities to discriminate between the sexes based on which sex provides care, it is worth looking at Fig 6.2. How confident are you about picking the male in these species? If you are less certain than you were before your trepidation is justified. Amphibians show a fantastic variety of forms of parental care and sexual division of parenting. In some species females lay trophic eggs to feed tadpoles, brood frogs inside their stomachs or carry developing frogs in fleshy capsules on their backs. Similarly, males sometimes guard schools of tadpoles, build canals to move tadpoles between temporary pools, or carry them to new site (Wells 2007). There are even species where males carry froglets on their backs (Bickford 2002). Biparental care is rare in anurans but male-only and female-only care have evolved equally often from a state of no care (Beck 1998; Reynolds et al. 2002; Summers et al. 2006). The caring frog parent in Fig 6.2 is therefore equally likely to be a male or female.

In teleost fish, the sex of the carer is more predictable, but this is because male-only care is found in nine times as many genera as female-only care (Gittleman 1981; Gross & Sargent 1985; Reynolds et al. 2002). Excluding livebearers, in fish taxa where phylogenies have been analysed for evolutionary transitions, female-only care is a more recently derived state, arising almost exclusively from biparental care (e.g. cichlids: Goodwin et al. 1998; Klett & Meyer 2002; Gonzalez-Voyer et al. 2008; ray-finned fish: Mank et al. 2005). Finally, while birds tend to show a female bias in parental care, shorebirds often show ‘sex role reversal’ with males caring for eggs and nestlings and females being larger, more aggressive and more brightly coloured than males (Thomas et al. 2007). Interestingly, if you had based your criteria for sex identification on the assumption that males invest more in courtship and mate attraction you might have been on safer ground. Even in frogs with male-only care it is still almost always the case that only males call to attract females. Likewise, in fish with male- only care, if there is sexually dimorphism, males still tend to be more brightly coloured than females.

Many non-biologists would probably have misclassified examples in figure 6.2 by assuming that females are always the primary carer-givers, a product of naïvely extrapolating from the still common norm in human societies. Even so, and despite variation in care roles in major taxa, among related species, and even within species (Trillmich 2010), our brief taxonomic review reveals a strong trend towards female-biased care in nature. This is true whether we consider the absolute number of species where female care predominates (given the sheer number of invertebrates), or the number of independent evolutionary transitions towards greater female than male care. In this chapter we will explain why females tend to provide more care, and what, on the other hand, maintains such fantastic diversity in outcomes.

6.2 Why does an individual’s sex predict its behaviour?

The predictable relationship between an individual’s sex and its breeding behaviour is most parsimoniously explained if there is something inherent to being a male or a female that applies across all taxa. We can immediately eliminate the mechanism of sex determination as a common denominator. The method of sex determination varies greatly among species: some have sex chromosomes, others are haplodiploid or exhibit temperature-dependent sex determination. The mechanism can even differ among populations of the same species (Pen et al. 2010). Moreover, even in species with sex chromosomes, females can be the heterogametic sex (e.g. ZW in birds and butterflies) or the homogametic sex (e.g. XX in placental mammals), and platypuses have a set of ten sex chromosomes.

Given this diversity, how do we decide to which sex an individual belongs? Why can we state with confidence that pregnant individuals are always male in seahorses even though the exact mechanism of sex determination is unknown (Tony Wilson, pers. comm.)? The answer is simple: biologists have agreed on a convention that individuals producing the smaller of two types of gametes — sperm or pollen— are called males, and those producing larger gametes — eggs or ovules — are called females. This classification works unambiguously for a far larger number of species than any other systematic sex difference because, when gamete size varies, it usually does so with strong bimodality (i.e. anisogamy). In species where different mating types are not distinguishable based on gamete size the terminology of two sexes — males and females — is abandoned. We then talk of sexual reproduction between isogamous mating strains, usually labelled + and –.

Armed with this information of what ‘being a male or a female’ means, we can now rephrase our earlier question about female-biased care: why is producing a small gamete associated with not providing additional parental care once gametes fuse to form a zygote? To answer this question it is important to understand the selective pressures that create anisogamy with a bimodal distribution of gamete sizes. In turns out that the reasons why a parent might be sparing in provisioning each gamete with resources have something in common with the reasons why the same parent might be less willing to subsequently invest in providing additional parental care. The resources in the gamete that are available to the zygote after fertilization represent the minimal level of parental care provided by a parent. A study of the evolution of gamete size is therefore simultaneously a study of the evolution of parental care. 6.3 The first sex differences in parental care: the evolution of anisogamy

There are several explanations for the evolution of anisogamy (see the excellent review of Lessells et al. 2009). One argument is based on elevating offspring fitness by reducing intracellular conflict. This favours uniparental inheritance of cellular organelles. Such uniparental inheritance does not, however, always occur through females. For example, although mitochondria are usually maternally inherited they are transmitted via sperm and pollen in several taxa (Cummins 2009). Here we focus on the more standard explanation that is also more closely linked to the male-female definition and the economics of parental investment. It is based on the economics of gamete production: reducing the investment in each gamete allows the parent to produce more gametes on the same budget.

This increase in gamete production is an example of the more general principle of a trade-off between offspring size and number (Lack 1947, Smith and Fretwell 1974, Lloyd 1987). From a parental perspective the optimal offspring size depends on maximizing the number of surviving offspring given a trade-of between offspring survival (which is assumed to be size- dependent) and parental fecundity. For example, if a mother in an egg-laying species could produce one very large offspring that survived to sexual maturity with a probability of 70%, or two medium sized offspring that each had a 40% survival probability, or three small offspring who have a 10% survival probability, the expected number of surviving offspring is 0.7, 0.8 and 0.3 respectively. Selection therefore favours the intermediate clutch size of two.

In general, optimality models for offspring size assume that only the mother determines their size. Sperm is assumed to make a negligible material contribution to offspring size, i.e., sperm are assumed to be tiny. When we turn our attention to the evolution of anisogamy, such an a priori assumption is clearly inappropriate. The number-size trade-off therefore involves additional considerations when the gamete size produced by either parent is free to evolve.

A gamete first has to survive until it finds a compatible gamete to form a zygote. Thereafter, zygote survival will depend on the combined effect of both gametes on offspring size. In a deviation from the simple optimization of the size-number trade-off, small gametes are not necessarily destined to give rise to offspring with poor survival prospects since they might fuse with large gametes. In effect, one of the mating types, which by definition we end up labelling as ‘male’, is selected to produce small gametes (sperm) to ‘parasitize’ the provisioning of the other mating type.

Consider a scenario where there is isogamy with + and – mating types. Initially mutants of one mating type that produce smaller that average gametes (a proto-male) will suffer a decline in offspring survival because this slightly reduces zygote size, but this is more than compensated for by the proto-males’ higher fertilization success, simply because they can produce more gametes. In turn, being fertilised by a smaller gamete selects for increased gamete size in the other mating type (proto-females) to ‘compensate’ for the decline in zygote size that begun with the evolution of sperm. Game theory models that make plausible assumptions about the size-number trade-off and the effects of gamete and zygote size on survival show that the resultant disruptive selection can readily drives the evolution of anisogamy (Parker et a. 1972, Bulmer & Parker 2002).

These classic models for the evolution of anisogamy do not explicitly model one consequence of altering gamete size: a gamete might never become part of a zygote. If one sex makes many more gametes than the other then most of these gametes are doomed to failure. This simple fact invokes the Fisher condition (Houston & McNamara 2005), named after R.A. Fisher who insightfully noted that since each offspring in a sexually reproducing diploid species has one genetic mother and one father, the total reproductive output of the two sexes must be identical at the population level. Fisher used this simple fact to explain the ubiquity of a 1:1 offspring sex ratio: if one sex is overproduced in the population then the other must have higher per capita reproductive success. The only stable outcome occurs when there is no such advantage to be gained, which is reached when parents invest equally into sons and daughters. If producing an offspring of either sex costs the same then the offspring sex ratio will be 1:1.

If genes from one individual of each sex are required to create a zygote, then the Fisher condition also means that the number of successful sperm must equal the number of successful eggs. In the case of gametes we never observe a 1:1 ratio of eggs to sperm. The size-number trade-off means that the sex with small gametes is producing a vast oversupply: most of these sperm are wasted. At first sight this makes the idea of ‘gametic parasitism’ by males seem less lucrative. If most sperm will not find an egg to parasitize, why does this not select for males to produce fewer, larger gametes? The answer lies in the trade-off between the likelihood of his gametes encountering other gametes to form a zygote, and increasing the survival of a zygote. When we produce a model for gamete size evolution that tracks the success of individual gametes and explicitly derives survival over time, isogamy can be maintained when gametes of both sexes are ‘reasonably likely’ to become a zygote (Lehtonen & Kokko 2011). Anisogamy evolves when there is a deviation from this ‘reasonable likelihood’ due to either a high encounter rate such that more numerous type of gametes compete locally for the less numerous type, or to a low encounter rate so that both gamete types struggle to find each other.

Why do such vastly different scenarios both lead to anisogamy? The answer can be visualised in terms of the strength of selection on proto-males to increase the number of their own gametes that will fuse with compatible gametes, versus the strength of selection to elevate the resultant survival of the zygote (i.e. increased parental care in the form of larger gametes). The combination of these two processes determines the net reproductive success of proto- males.

In a high encounter scenario (e.g., a broadcast spawner in a small body of water with many spawning parents) any numerical imbalance between smaller and larger gametes implies a situation akin to sperm functioning like tickets in a raffle where a limited number of prizes are guaranteed (the eggs are there). The only way to do better than other participants is to have more tickets. Admittedly this is an unusual raffle: each participant can be visualised as being given a piece of paper which he can cut up to make as many tickets as he wants. Succeeding in this stage of competition — the sperm competition stage — is a better predictor of male reproductive success than ensuring that the resulting zygote has a greater chance of survival. Increased zygote survival would still be beneficial, but it is difficult for a male to elevate this component of fitness economically. If a male is to increase the amount of parental provisioning he has to put extra energy into every sperm because the male cannot predict in advance which of his ‘tickets’, if any, will win a prize. Most of this parental care would be wasted because few of his sperm will locate an egg. Later in this chapter we will return to the problem of determining whether or not male care will yield dividends, as it is equally relevant for considering post-zygotic male parental care when paternity is uncertain as it is for pre-zygotic provisioning. Why does the opposing scenario of low gamete density also select for anisogamy? The need for a male to increase the likelihood that one of his gamete locates an egg before a rival’s gametes is now replaced by the task of simply locating an egg. The advantage of producing numerous sperm now comes from raising the likelihood that at least some sperm will find an egg. The analogy with a raffle with a guaranteed prize is no longer valid (some prizes are never found); perhaps a better analogy is putting up many reward notices around your neighbourhood in the hope that one will be read by the person who has found your missing cat. Females are no longer victims of parasitism: they too benefit from males producing numerous, albeit small, sperm because some of their eggs would otherwise fail to be fertilized. It is an obvious question to ask why eggs do not evolve to be small too, because the largest absolute number of fertilizations might well occur if both sexes evolved very small gametes. This solution is not feasible, however, as the resulting small zygotes would have very low survival prospects. Given that both gamete type cannot simultaneously evolve to be very numerous and very small, there is even the potential for selection for bigger eggs to provide a larger target for sperm (Levitan 2006).

In summary, the most basic form of parental care is the provisioning of gametes that determines initial zygote size. Male parental care is reduced due to sexual selection to locate unfertilized eggs. Returns on parental investment remain low if difficulties in finding eggs to fertilize mean that most of the investment is wasted. This can happen either because unfertilized eggs are rare (low density), or because of the presence of rivals who compete to fertilise eggs.

6.4 What happened next? Sex roles in post-zygotic parental care

The previous scenarios are usually envisaged as eggs and sperm being released into an aquatic medium so that the zygote forms away from parents. If so, anisogamy means that the female is by definition the primary care provider. This book would not exist, however, if the story ended there. Post-zygotic care of offspring has evolved numerous times in both external and internal fertilizers. Minimally, however, its evolution requires that the male and/or female parent can locate zygotes formed from their gametes. In internal fertilizers, the zygote is initially surrounded by parental tissue (e.g. the brood pouch of a male seahorse after the female has inserted her eggs, or the reproductive tract of a female guppy after a male has inseminated her). Whichever sex provides this tissue is in a better position to continue to provide care. In this sense it is unsurprising that, say, female mammals provide more post- zygotic care than males. Given gestation and live birth females have the option to provide additional energy resources to their offspring through a placenta (for placental evolution in fish see Pollux et al. 2009) or post-birth provisioning in the form of lactation. If the males remain nearby, however, there is no obvious barrier to prevent him from evolving the ability to lactate (Hosken & Kunz 2009, Kunz & Hosken 2009). Males have the same basic physiological and morphological trait required for lactation as females (Wynne-Edwards & Reburn 2008). Similarly, when fertilization is external and eggs are laid onto the substrate both parents are present when zygotes form.

Seahorses are a reminder that ‘pregnancy’, or more broadly ‘baby-carrying’, are not a priori tasks exclusively performed by females. Either sex could take sole responsibility for carrying and/or guarding fertilized eggs, especially when there is short interval between fertilization and zygote availability (e.g. in external fertilizers). Nothing in principle prevents the male from doing this: male frogs transport tadpoles to water; in Belastomatid water bugs females cement fertilised eggs onto the male’s back (Inada et al. 2011); and male-only guarding of fry occurs in numerous fish (Mank et al. 2005). One approach to explain current differences in male and female care is therefore to focus on environmental or social factors that influence the likelihood each parent will encounter its own offspring, while treating existing sex differences (e.g. female gestation) as constraints. For example, post-zygotic male care might be related to whether or not there is sufficient food for a female to be able to remain on a male’s territory during pregnancy. This kind of explanation is often instructive to account for special cases such as sex role reversal in taxa where females usually provide the bulk of.

These explanations invoke already existing constraints (sex biases), however, so they are insufficient for explaining the general trend for females to provide more post-zygotic care than males. We are primarily interested in working from first principles, rather than invoking ecological and phylogenetic contingencies. We want to determine why selection in most taxa favours the large gamete producer remaining with zygotes, rather than taking this as given. In other words, gestation in mammals seems to predispose females to be the sole care-givers, but this only raises the question why females rather than males evolved the ability to gestate. Ancestral sexual asymmetries in parental care can constrain much of the subsequent variation we observe among extant species, but they in turn must also be explained. So, leaving aside whether one sex is more likely to be physically present when zygotes form, what else might explain a bias towards greater female care?

An obvious point to make is that any explanation for why females care more than males must take into account the potential for sexual conflict over caring (Lessells 2006; Johnstone & Hinde 2006; Olson et al. 2008). Unless there is lifelong monogamy each parent would probably do better if it could convince the other parent to bear the full costs of caring. Indeed, many behavioural studies investigate species where one sex compensates by caring more when the other sex cares less, so that survival of the young is only compromised to some degree. The short-term stability of biparental care is largely based on the assumption that any such compensation is only partial, as complete compensation would favour immediate desertion by one parent. In general this assumption seems valid (Harrison et al. 2009). There is often an emphasis on symmetry when parents are ‘negotiating’ levels of care: individuals of either sex benefit from caring less or, in extreme cases, deserting the brood first so that the other parent has to care alone (Szentirmai et al. 2007). In a longer term evolutionary perspective (which might no longer involve a negotiation over biparental care if one sex does not provide care), this raises the question of why it is so often the male who deserts and leaves the female with the brood.

Most empirical studies of parental care are based on a comparison of the costs/benefits of caring versus deserting, making the assumption that these can be detected because both sexes adaptively adjust their behaviour to maximise their fitness. This allows us to infer how specific factors affect these costs/benefits for each sex (e.g. Jennions & Polakow 2001), while taking into account that how the other sex responds affects the cost of providing less care. In an evolutionary context, however, we must ask how changes in the mean behaviour of each sex affect the fitness of the other, creating selection pressure for changes in each sexes behaviour until an evolutionary stable state is reached where individuals of neither sex can improve their fitness by behaving differently.

In the following three sections we provide a non-mathematical account of recent models that account for the evolution of female-biased care, as well as for variations around this theme. Our account is mainly based on the arguments of Queller (1997) and the subsequent modelling and extension of these ideas by Kokko & Jennions (2008). We start by explaining what factors select against male care. Second, we discuss factors that limit the fitness gains males can achieve by caring less. These limitations help explaining why male care or biparental care can evolve while an overall female bias towards greater care-giving still persists.

6.5 Uncertainty about parentage reduces male care

Earlier we stated that anisogamy results in sperm vastly outnumbering eggs. There are two assumptions behind this statement. First, that there are not many more female than male adults currently trying to breed. Second, that the total budget each sex invests into gamete production is of a similar size. If, for example, each male only produced a few sperm or there were very few males releasing sperm per receptive female then sperm would not outnumber eggs. Given that the selection driving anisogamy results in an enormous size difference between eggs and sperm this would, however, require very large deviations of the breeding sex ratio towards females and/or towards greater female than male reproductive investment before sperm become rarer than eggs. Thus, the numerical asymmetry is fairly robust: sperm compete to locate eggs before their rivals, rather than eggs participating in a similar competition for sperm. Of course, the numerical abundance of sperm does not make sperm competition inevitable. For example, there are insect species where females only seem to mate once (Arnqvist 1998) and males still produce small sperm. There is, however, some evidence that there is then natural selection for males to produce fewer and/or larger sperm (e.g. Simmons & García-González 2008). Also, as already discussed, very low adult densities in a broadcast spawner have the comparable effect of eliminating sperm competition (Levitan 2010).

Exceptions aside, given the numerical abundance of sperm, it is likely that sperm from several males are present near the same egg shortly before fertilization. This creates uncertainty as to which male has sired a zygote. This statement is certainly true when fertilization is external and it remains true with internal fertilization if females also mate multiply (which is almost always the case; Slatyer et al. 2011). The female situation is different. Eggs are rare, so when a female remains in the vicinity of her eggs there is typically little likelihood that she will mistake the eggs of another female for her own. Once again, there are exceptions. Egg dumping occurs in some birds (Petrie & Møller 1991) and insects (Tallamy 2005) and, in extreme cases, eggs that a female might consider her own are actually those of another species (e.g. cuckoos). When there is communal spawning by females the mixing of eggs also makes it difficult or impossible for females to know which zygotes are their offspring. Still, since sperm are more numerous than eggs, there is a sexual asymmetry in that male are more often in situations where they are uncertain about a zygote’s parentage than are females. Although we will stick to convention and talk about how ‘uncertain parentage’ (usually uncertain paternity) lowers the benefits of caring, it is actually the certainty of the decline in mean relatedness to putative offspring that matters. For example, if sperm from three males is released when a single female spawns it must follow that the average reproductive success of these males is a third of a clutch.

Across species, or between the sexes, higher uncertainty of parentage decreases the benefit of caring. Unfortunately, the literature on how confidence of paternity relates to male care is built around questions concerning phenotypic plasticity of individuals within a species (i.e. adaptive shifts in the extent of male care over his lifetime). It is easy to become confused and question the validity of our statement. Before dealing with some of the sources of confusion, we would like to reassure the reader by presenting a few simple questions. If the only benefit of caring is to increase the survival of one’s own offspring, should a male who has no paternity in a brood provide care? (Answer: No). Is the maximum benefit gained from caring linearly related to the proportion of offspring in a brood that are your own? (Answer: Yes). So, if species vary in the mean uncertainty of paternity (certainty of siring fewer offspring in each brood), and nothing else, is the maximum benefit of care lower for males when uncertainty is greater? (Answer: Yes). So, if females have a lower uncertainty of parentage than males, is the maximum benefit of caring greater for females? (Answer: Yes). All that is then required is to realise that any function relating caring to its benefits must asymptote at a maximum: at the extreme, caring cannot ever increase offspring survival beyond 100%. If each sex provides the same quality of care, the lower maximum benefit of caring for males must mean that the marginal benefits from additional care decline, at some point at least, more rapidly for males than females.

So, why might one be confused about the relationship between the certainty of paternity and male care? There are at least three sources of confusion, which we deal with below.

6.5.1. Why exactly does paternity matter?

It is easy to fall into the trap of arguing that paternity should not matter when lifetime fitness depends on balancing current and future reproduction. If paternity is likely to be higher in a future breeding attempt, then selection might favour ‘saving’ energy to invest more into one’s own survival and future care. If a male consistently has the same likelihood of paternity, however, his current reproduction has been argued to be devalued by the same amount as his future reproduction, implying that across species average paternity will not matter when determining the mean level of male care (Maynard Smith 1977). The flaw in this argument is that it neglects the fact that males gain offspring not only in broods for which they care, but also by siring extra-pair young (Queller 1997; Houston & McNamara 2002). The flipside of lost paternity is that extra-pair mating opportunities must exist elsewhere. Because these opportunities are part of a male’s future reproductive success (but are not included in the fitness gains from his current brood), low paternity, even if it is consistent across broods, does not have equivalent effects on a male’s current and future reproduction (Westneat & Sherman 1993, Queller 1997, Houston & McNamara 2002

Support for a relationship between lower than average paternity and a reduction in parental care (or even greater ‘anti-care’ in the form of offspring cannibalism) can be found in within- species studies on phenotypically plastic male care (e.g. Neff 2003; Gray et al. 2007). It is worth noting that tests for a negative effect of paternity on male care should not look at the correlation across males. For example, unattractive males might have consistently low paternity but, if they have no ability to gain extra-pair matings, their best bet might be to invest more in care than do attractive males. Ideally one requires a comparison of changes in care by a male when his current share of paternity differs from his future expectations (which might be the population average, or an expectation based on the male’s own life history circumstances). This is ideally achieved by experimentally manipulating a male’s perceived share of paternity, which could also require a change in actual paternity if males can assess paternity directly (e.g. Neff 2003). Given that we are primarily interested in the evolution of care patterns given selection on the mean levels of investment by each sex, it is also important to pay attention to phylogenetic studies. In birds these show that male parental care is lower when extra-pair paternity is high (Møller & Birkhead 1993; Møller & Cuervo 2000). This is an encouraging sign that paternity has a strong influence on male care, because mean paternity can depend on other traits that might also affect male care, so that the reverse relationship could arise (Houston & McNamara 2002). 6.5.2. Behavioural and evolutionary timescales are not equivalent

A common source of confusion is the tendency to ignore differences in how selection can act over behavioural and evolutionary timescales. The average paternity in a population influences male care decisions because male possess ‘evolutionary knowledge’ about their expected paternity, based on strong selection in the past to provide a level of care that maximizes fitness. Simultaneously, a male’s likelihood of being the parent of a given offspring can differ from the average male in the current generation (or even his own lifetime average). This is why it is dangerous to test the selection imposed by factors of interest (e.g. level of paternity) by assuming that behavioural or other phenotypic responses will mimic the predicted evolutionary response to selection. More specifically, how do we interpret failure to detect a behavioural response to low paternity? It could mean that the focal factor does not select for the predicted traits (i.e., lower paternity does not select for reduced care), or that selection for adaptive phenotypic plasticity has been insufficient, perhaps because the relevant cues or the ability to detect these cues do not exist to elicit an adaptive behavioural response. These are not equivalent explanations. The former case would force us to question whether our theoretical predictions are valid, the latter merely raises issues about constraints on selection.

Failure to distinguish between how selection acts over behavioural and evolutionary timescales is surprisingly common. It can easily lead to claims that female will pursue mating strategies that promote the evolution of desirable male traits in the other sex. For example, Morton et al. (2010) argued that, “genetic monogamy [...] may be a female tactic that reduces the likelihood of males evolving counter-adaptations to female desertion”. Although it seems self-evident that individual selection cannot favour traits that reduce undesirable evolutionary outcome for other females who exist in the future (except as a fortuitous by-product of other selective processes), this type of reasoning is sufficiently common that it is worth drawing attention to it (the weakness of a similar argument is discussed by Kokko & Jennions 2010).

The existence of cues to detect deviations from prevailing parentage certainty is particularly pertinent when considering how loss of paternity generates sexual conflict over care (Kokko 1999, Mauck et al. 1999). To illustrate the importance of behavioural and evolutionary timescales, and the presence and accuracy of cues that allow for adaptive behavioural responses, consider a species with biparental care where females sometimes engage in extra- pair matings. If a female could signal to her mate that his share of paternity is above the current norm in the population (i.e. the average over recent evolutionary time) she might induce him to provide more care (Shellman-Reeve & Reeve 2000). Such a signalling system is, however, unlikely to be stable. All females would benefit by signalling to their mate that he had above average paternity. Instead selection is more likely to favour females who conceal information about paternity, even though males would benefit from an honest signal.

If males do not detect deviations from mean paternity that occur over behavioural time then within each generation females do not pay the cost for mating multiply that would arise if males adaptively reduced their care (Kokko 1999). Selection on male parenting decisions will therefore only depend on evolutionary knowledge of the long-term average paternity in the population. This means that very small net benefits are enough to favour extra-pair mating (Slatyer et al. 2011), even though they will make paternity decline over evolutionary time. Despite the absence of within-generation selection on females not to mate multiply, mean male care will still decrease over evolutionary time because of evolutionary knowledge of the decline in paternity. If female become sufficiently promiscuous (or actively bias paternity towards extra-pair males, e.g. Pryke et al. 2010), a possible evolutionary outcome is that females end up as the sole caregivers (Kokko 1999) (Fig 6.3). This could result in a decline in mean female breeding success representing a ‘tragedy of the commons’ (Rankin et al. 2007). Females evolve to lose a valuable resource (male parental assistance) because no female within any generation pays the price for her actions.

6.5.3. Traits that protect paternity can coevolve with care

It can be challenging to establish the casual link between paternity and parental care if care coevolves with traits that protect a male’s paternity (Kvarnemo 2006). What if there are male traits that function to safeguard paternity that also enhance offspring survival? Or, what if sexual selection for traits that increase male care has the by-product of increasing paternity? If such traits exist, selection will lead to male care being greater than expected if we only considered responses to changes in paternity arising from factors uncorrelated with male care itself.

Protecting paternity involves better defence of unfertilized eggs (e.g. pre-copulatory mate guarding), while enhancing offspring survival is mostly dependent on process that occur after zygotes have formed. Thus, arguing that care can evolve as a correlated response to paternity protection requires that the relevant traits are able to bridge this temporal gap. Kvarnemo (2006) lists a range of intriguing possibilities as to how this might happen. For example, nuptial gifts or courtship feeding can increase sperm uptake by females (increasingly a male’s likely share of paternity) while also providing more nutrients for offspring. Similarly, in fish, a well built nest might improve a male’s ability to gain paternity as well as making offspring better defended. Current male care could also affect paternity in future breeding events. For example, males might repeatedly breed with the same female and her propensity to engage in extra-pair matings might be lower when the male has provided more care during the previous breeding event.

A mechanistic explanation for a link between a male’s ability to gain paternity and to provide care is that there are ‘constraints’, possibly mediated by hormonal trade-offs (McGlothlin et al. 2007), that lead to behavioural consistency in different contexts (e.g. Royle et al. 2010). For example, males that are more attentive at mate guarding might have a greater propensity to aggressively defend offspring against predators. The ideas of Kvarnemo (2006) appear to be worthy of further study, not least because any factor that keeps parents near putative young is a prerequisite for the future provision of care.

6.6 Don’t bother caring till the going gets tough: the OSR

Although the primary sex ratio is usually near 1:1 due to the Fisher condition generating negative frequency-dependent selection on the returns per offspring of each sex, there is no selection to maintain sex ratio equality after parental care has ended (West 2009). Dramatic differences in mortality between the sexes are possible. How then does the adult sex ratio (ASR) affect parental care by each sex? This is an important topic as recent theoretical work reveals some counterintuitive outcomes. A persistent theme in the literature has been the claim that whichever sex experiences difficulties in finding mates will benefit from investing more heavily into mating effort (Trivers 1972; Dawkins 1989; Clutton-Brock & Parker 1992). This has been interpreted to mean that, by implication, this sex will not gain equally much benefit by providing more parental care. The difficulty of finding mates is usually expressed as the operational sex ratio (OSR): the ratio of sexually available males to females (Emlen & Oring 1977). The OSR takes the ASR as its baseline, but modifies it by removing all individuals who are currently unavailable as mates because they are caring for young and/or replenishing resources required to mate and breed again. Individuals who are ready to mate are said to be spending ‘time in’ the mating pool, the rest are spending ‘time out’ (Clutton-Brock & Parker 1992, Parker & Simmons 1996). There is therefore no guarantee of a linear relationship between the OSR and ASR because sex divergence in parental care is a major determinant of the OSR in a way that is not for the ASR (We note, however, that if there are sexual differences in caring and ‘time in’ and ‘time out’ activities have different mortality rates this will result in sex differences in mortalities than affect the ASR. We will return to this issue in Section 6.7.).

The notion that difficulty in acquiring mates favours greater mating effort and less parental care suggests that any initial bias in the OSR will be self-reinforcing over evolutionary time until the rarer sex in the OSR is the sole provider of care. According to this logic, self- reinforcement happens because if sex A cares slightly more than sex B this increases its ‘time out’ so that A becomes rarer in the mating pool. Sex B is then assumed to respond to the intensified competition for matings by investing in traits that increase the likelihood of mating. This diverts resources away from caring in sex B which, in turn, further selects for greater care by sex A. This further increases the bias towards B in the OSR until eventually sex A provides no care. If there is any initial bias favouring slightly greater care by one sex, then this sex will eventually be the sole caregiver.

There is an obvious empirical problem with any account that makes strongly divergent care roles appear inevitable: in reality, biparental care exists. Sometimes such cases can be explained by the benefits of synergy. Care models predict, rather unsurprisingly, that biparental care is more likely if two parents perform parental duties more efficiently (i.e. greater offspring survival per unit of care) than either parent caring alone (Kokko & Johnstone 2002). The real problem, however, is that the self-reinforcing process relies on an effect of the OSR that, when explicitly modelled, appears problematic. Numerous models have shown that an overabundance of males selects for more male care (Yamamura & Tsuji 1993, McNamara et al. 2000, Houston & McNamara 2002, Kokko & Jennions 2008). Similar conclusions have been reached for other male traits that increase fitness by remaining with the current mate. For example, selection for mate guarding a female to protect paternity, rather than seeking out other females, becomes stronger in more male-biased populations (Carroll & Corneli 1995, Fromhage et al. 2005, 2008). In hindsight, it is obvious that a male is more likely to desert a current female or his young when there are more, not fewer, reproductive opportunities available elsewhere, i.e. when the OSR is female-biased.

It is now worth recalling the insights gained from considering gamete size evolution. Gamete size can show self-reinforcing divergence due to the greater abundance of sperm than eggs. Why then does male abundance (in the OSR) not inevitably lead to a similar divergence where the OSR becomes ever more male-biased? Instead, models predict that the difficulties of securing additional matings make the male more likely to care. The solution depends crucially on the seemingly trivial fact that a male is only in a position to provide care once he has mated and his potential offspring exist. We noted earlier that anisogamy evolves under sperm competition because “the male cannot predict in advance which of his ‘tickets’, if any, will win the prize”. Contrast this with the evolution of post-zygotic male care, and assume that the level of paternity is p (between 0 and 1). We can now ask how the expected future number of reproductive opportunities with other females will influence whether the male should continue to care to improve offspring survival, or desert and seek a new mate. A male in a male-biased population experiences a trade-off between investing in offspring that already exist and investing in gaining future ones that might never exist. Caring for existing offspring offer an assured fitness return that remain unchanged (albeit discounted by p given uncertain parentage) as future mating opportunities become scarcer, while the return from future offspring is weighted by the likelihood of securing a mating. Securing a mating is clearly more difficult when the number of competitors per female increases. For the same paternity certainty p, a male will gain relatively more by improving the survival of his existing young if securing additional matings becomes more difficult. This is why a male- biased OSR selects for male care. Some of his current paternal investment is wasted if parentage p is less than 100%, but this is less waste than that experienced at the gamete production stage. The abundance of sperm and intense competition for eggs favours reduced pre-zygotic male care because a male cannot direct parental care towards the few sperm that will end up with above average success in the same way that he can direct paternal care towards already existing offspring.

In sum, a numerical bias in gametes towards sperm tends to create sperm competition, reduce the per-sperm investment and lead to anisogamy (i.e. low pre-zygotic male care). Sperm competition, by reducing the certainty of paternity, also selects against post-zygotic male care. Intense pre-copulatory competition for mates (a male bias in the OSR), however, favours greater post-zygotic male parental care. The same argument applies for females when the OSR is female-biased. The Fisher condition tends to equalise the level of post-zygotic male and female care, and it can explain why biparental care can exist even if synergistic benefits of care are absent. If one sex cares for longer (or provides more resources so that it takes longer to recover) it spends more time out of the mating pool. The opposite sex therefore experiences difficulties in securing a mate when it returns to the mating pool. This, in turn, selects for it to do something else that raises fitness (e.g. provide more care). This negative frequency-dependent selection offers a plausible explanation why sex roles do not always diverge to the extent that only one sex cares.

6.7 Orwell was right, not all animals are equal: sexual selection and the adult sex ratio

If uncertainty of parentage and biased operational sex ratios were the only factors driving parental care, we would predict that female multiple mating or group spawning select for reduce male care, and that this is countered by frequency-dependent selection due to the negative effect on male mating opportunities. The process is not self-reinforcing. Uncertainty of parentage can easily promote a modest sex bias in levels of care (e.g. Fig. 3c in Kokko & Jennions 2008), but the Fisher condition makes it difficult to explain uniparental care. This is analogous to factors such as differences in production costs of each sex that select for a biased primary sex ratio, but the inevitable frequency-dependent selection on the sex ratio (again due to the Fisher condition) always prevents one sex from being completely absent. How, then, do we account for uniparental care being so common in nature? Aside from very low paternity prospects for males (Fig 6.4), what other explanations exist?

One complication missing from the preceding explanations is that not all individuals of a given sex in the mating pool experience the same level of competition. The Fisher condition dictates that the more numerous sex in the mating pool must, on average, have a slower mating rate than the rarer sex. Even so, some individuals of this sex could still have a reliably high mating rate. Sexual selection acts on traits that increase success when competing for mates (or, more accurately, for access to gametes of the opposite sex). Individuals with traits that are favoured by sexual selection will spend less than the average time for their sex in the mating pool. Crucially, only individuals that mate are ever in the position where their propensity to provide care is exposed to selection. Only they, having mated, have young that they can apportion care to. Should these successful individuals care or desert?

If sexual selection is strong, mating per se indicates that an individual bears traits that will also lead to above average mating success in the future. These individuals are less strongly affected by the Fisherian frequency-dependent selection that inevitably lowers the mating rate of the sex that is more common in the mating pool. Consequently, they will sooner reach the point where they can gain more by returning to the mating pool than they can gain by continuing to provide care.

Mating systems are usually defined by a combination of the sex-bias in parental care, the intensity of sexual selection on each sex, and the level of multiple mating/group spawning. These factors are all related to each other because, as we have shown, sexual selection and uncertainty of parentage influence the sex-bias in parental care. If sexual selection is sufficiently strong, it can seemingly counter frequency-dependent selection due to the Fisher condition. Mated individuals of the sex that is common in the mating pool can benefit from providing no care and deserting their young to try and mate again, if they possess traits that make their mating success repeatable. Depending on the relative strength of sexual selection, the system can shift from biparental care with a mild sex bias to totally uniparental care (see Kokko & Jennions 2008 for numerical examples). The Fisher condition never actually disappears, but with strong enough sexual selection, it no longer constrains the mated individuals of the more numerous (less caring) sex in the mating pool to have a lower mating rate than that experienced by the less numerous (more caring) sex.

The central role of sexual selection in determining parental care us makes it important that we can measure the strength of sexual selection, see which individuals it favours, and contrast this with the average difficulty of gaining matings experienced by an individual of that sex. The OSR is directly related to the latter average, but less clearly to the former. It is tempting to assume that sexual selection is always stronger on the sex that is more common in the mating pool (Emlen & Oring 1977), but this is false. When there is a biased OSR the mean mating success per time unit is low for the more common sex, but it does not follow that we can equally easily assert that mating success in this sex will depend strongly on any particular trait. Ultimately a causal link between a trait and the ability to acquire fertilization defines sexual selection. This strict definition is essential for an individual’s mating success to be repeatable which, as we have seen above, is needed to explaining patterns of care that deviate from a small amount of variation around biparental care. Without traits that repeatable increase mating success, a mated individual cannot assume it will have high mating success after deserting its current young and avoid the full force of Fisherian frequency-dependence which otherwise leads to biparental care.

It might often be true, but is unwarranted to simply assume that the bias in the OSR predicts the strength of sexual selection (Fitze & Le Galliard 2008, Kokko & Jennions 2008, Klug et al. 2010). For example, sexual selection has been shown to either intensify or diminish as the absolute density of individuals increases (Kokko & Rankin 2006). If density-dependence has different effects on how the mating success of each sex depends on specific traits then, for a given population density, a change in the OSR could increase or decrease sexual selection on each sex (Klug et al. 2010). The relationship between the OSR and sexual selection has to be determined empirically but to date, very few studies have quantified this relationship (Fitze & Le Galliard 2008). In particular, there are surprisingly few experimental studies that manipulate the OSR and document sexual selection on focal traits (or relevant proxies; see Weir et al. 2011). Studies documenting changes in variance in mating success are a poor substitute because selection acts on traits and variance can be high due to purely chance events (Sutherland 1985).

Understanding how the OSR related to the strength of sexual selection is crucial to account for sex-biased parental care. If sexual selection intensifies with an increased bias in the OSR, then mild initial biases in care become self-reinforcing. Successful members of the more common sex in the mating pool will comprise an ever smaller subset of that sex. This means that they are unaffected by the increasing bias in the OSR that lowers the mating rate for the average individual of their sex. They can keep on deserting their young and maintain high fitness by seeking out more matings. If, however, sexual selection saturates or even declines at a high OSR (e.g. because it is impossible for a male to monopolize matings when there are many competitors, Klug et al. 2010) then the subset of successful males becomes larger. The per capita decline in mean mating rate with an increasingly biased OSR affects more of these males, thereby selecting for greater male care.

In our view, one of the most interesting feedbacks between sexual selection, sex ratios and parental care could operates through the relative mortality costs of caring and competing. The ASR sets the baseline for the OSR. The OSR is the ASR corrected for the difference in care by each sex that determines their ‘time out’ of the mating pool. Any factor that influences the ASR will therefore shift the balance of the forces that determine the level of male and female care. But what if sex differences in care themselves affect the ASR? Parental care and competition for matings are often dangerous activities (Liker & Székely 2005) and/or require initial investment in traits that can later affect mortality (Moore & Wilson 2002). If caring is a more life threatening activity than an alternate activity such as mate searching, then whichever sex cares more will become rarer in the population. This, all else being equal, will — perhaps counterintuitively — select for the opposite sex to care more: being a member of the overrepresented sex means that future mating opportunities are scarce. If, however, seeking out mates is a more dangerous activity (costs of sexual competition are often severe) then the sex that spends less time caring and more time in the dangerous activities of the mating pool will become rarer in the ASR. All else being equal, surviving members of this sex then have a relatively greater number of mating opportunities.

The outcome of a scenario where the more caring sex is rare is reminiscent of patterns seen in many bird species: they tend to have a male-biased ASR and biparental care — nicely fitting with the idea that the Fisher condition makes males less optimistic about securing matings elsewhere when males are common (while extra-pair paternity can conceivably explain the slightly greater female investment per brood). Intriguingly, bird species that lack male care tend to have a female-biased ASR (Donald 2007), which resembles the typical situation in mammals. In most mammals male care does not occur and there is often high male mortality (usually attributed to male investment in traits that will increase mating success) (Wilson & Moore 2002) so that the ASR is female-biased. In such a setting, males — especially those who have already proven their ability to gain matings by siring young — can be relatively optimistic about their future mating success, and are unlikely to benefit as much by caring for young. Even though the lack of male care might, depending on the ASR, lead to a strongly male-biased OSR, the Fisher condition reminds us that each baby produced has been sired by a living male, which makes the mating optimism of males appropriate. 6.8 Conclusions

We have sketched a general outline of why females care more than males but, as every evolutionary biologist knows, contingencies of history can result in taxon-specific traits that sometimes seem to rewrite the rules. When observed outcomes disagree with the predictions of theoretical model it is, however, often prudent to check whether the model’s assumptions hold in the study system rather than automatically assuming the model is fatally flawed. An interesting case study is the common occurrence of male-only care in many fish. We have assumed that there is trade-off between caring and re-mating. This is a valid assumption in many taxa. In fish, however, this does not seem to hold because parental care involves activities such as nest defence and egg fanning that can be performed almost equally easily for a few or many offspring (Stiver & Alonzo 2009). Males are therefore willing to receive additional eggs from new mates. Females appear to be willing to lay eggs with already mated males because the presence of eggs is a sign that the male is a good parent and/or is attractive to other females (so might have attractive sons) and/or because the per capita risk of predation or even cannibalism declines when a male guards more eggs. Little or no increase in parental costs when caring for many zygotes can also explain some seemingly counterintuitive results. For example, despite our general argument that uncertainty of paternity will lower care, male care increases with lower paternity in the ocellated wrasse Symphodus ocellatus (Alonzo & Heckman 2010). This makes sense, however, if the male is still caring for an absolutely greater number of offspring that he has sired, and the costs of caring are not rising in direct proportion to their number of young.

Even so, there are still many taxa where it is a challenge to work out why only one sex cares, and why it is the sex that it is. For example, many frogs seem to have rather similar breeding systems and comparable ecological requirements so why within the same genus do only males provides care in some species and females in others? Likewise, mouthbrooding in fish would seem to place limits of mating rates, so why does male-only care still occur? Can these differences be explained by ‘tipping points’ within the framework we have provided? For example, that small ecological changes result in large shifts in the strength of sexual selection, the degree of multiple mating or the adult sex ratio. Or do they depend on taxon- specific traits that might not be not readily applied across taxa. For example, that females prefer males providing care as in fish (but see Tallamy 2000 for evidence of a similar preference in insects). Or are these outstanding general factors that are missing from the current theoretical models?

One of the exciting areas we see is the attempt to empirically test the model we have outlined. This is a challenging task, however, because – as we have noted – we are making predictions about evolutionary responses and these do not necessarily have to be mimicked when making comparisons between parents in different environments (i.e. adaptive plasticity). This places limitations on the extent to which behavioural studies of extant variation in care can be used to test models. Cross-species studies are more powerful and there have been a few attempts to conduct phylogenetic tests to see whether transitions between different major patterns of parental care can be predicted based on the level of sexual selection (e.g. Gonzalez-Voyer et al. 2008; Olsson et al 2009). Again, however, because phylogenetic studies report correlations we need to analyses them cautiously as species often differ in several respects.

Ideally, we would like to run experimental evolution studies akin to recent ones in which lines are assigned to monogamy and polyandry treatments and trait evolution is then monitored (e.g. Simmons & Garcia-Gonzalez 2008), but with a focus on parental care. One could, for example, establish selection lines in which the adult sex ratio is made either heavily male-biased or female-biased each generation. The obvious problem is, however, identifying suitable species with a sufficiently short generation time and readily measurable care. More pragmatic, perhaps, is to rely on ‘natural experiments’ by investigating differences among populations in key factors (e.g. the adult sex ratio or level of paternity) and then testing whether the predicted pattern of parental care occurs. Although we can never be sure that the factors in question are driving the differences this does at least provide one way forward. As an interesting example, we recently noted a dataset that focused on variance in male and female mating success in different human populations (Brown et al. 2009). Populations were classified as polygynous, serially monogamous or monogamous. The level of male care per female is presumably lowest in the former and highest in the later. If the mean reproductive success of males and females is assumed to be correctly estimated then, given the Fisher condition, the inverse of this ratio is a measure of the ASR. There was a significant difference in the ASR between the three social systems (Fig 6.4).

Finally, we end with a strange piece of natural history that reminds us that nature always throws up challenges when we try to come up with grand theories unified by common themes. We have made much of the Fisher condition – one mother and one father. Even this ‘fact’ is, however, violated in at least one diploid sexually reproducing organism – and a primate no less. Marmosets Callithrix kuhlii live in polyandrous groups with two males caring for offspring. Fascinatingly, they are sometimes chimeric with siblings exchanging cells in utero. As a result, one offspring has two fathers and, more importantly, from an evolutionary perspective, the germ line tissue is also chimeric so that either father’s genes might be transmitted to the next generation (Ross et al. 2007). Amazingly, the more chimeric offspring were tissues that males could detect, the more they were carried by males, presumably because offspring scent profiles match both fathers. This is the kind of wonderful quirk of natural history that reminds us how easily the limits of our own imaginations can sometimes constrain our ability to solve problems. That said, we are still confident that paternity, sexual selection and adult sex ratios will continue to predict parents of parental care.

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IMAGES ARE JUST TO GIVE GENERAL IDEA.

Figure 6.1 Which is the male and which is the female? (Figure will comprise need a male and female bird, mammal, reptile and invertebrate)

FIGURE TO BE MADE

Figure 6.2. Which is the male and which is the female? (Figure will comprise a male and female fish (mouth brooding cichlid?) poison dart frog and shorebird/wader).

Figure 6.3 Predictions of evolutionarily stable care effort by females (circles) and males (squares) when females can either mate with their social mate (’faithful female’) or multiply (’unfaithful female’), and males can to some extend detect female mating behaviour but this is either relatively inaccurate (A) or relatively accurate (B). Evolutionary changes occur along the x axis, behavioural responses along the y axis. Males possess evolutionary knowledge of average female behaviour, and multiple mating by females selects against male care (which always declines with the proportion of multiply mating females). Whether multiple mating is selected against or not in females, however, depends on the fitness difference between unfaithful and faithful females (vertical differences between circles in the female fitness graph). Males paired to unfaithful females tend to be suspicious but some of them remain unsuspicious, and males paired to faithful females tend to be unsuspicious but some of them become erroneously suspicious. When the accuracy of cues is low (case A), errors in such judgments are common. Consequently males are not selected to put much weight on behavioural evidence, and the care effort between the different types of males remains largely similar at each point in time. The mating system fails to penalize unfaithful females sufficiently to prevent multiple mating from spreading. The horizontal arrows, depicting female evolution over time, show that the proportion of multiply mating females approaches 1, and male care is entirely lost from the system. Selection works against female multiple mating only if females of each generation lose a large amount of male care by being unfaithful. This occurs in the middle region of (B), indicated by the arrow pointing left, but not elsewhere. Even (B) will evolve towards more multiple mating if the population starts out from a point where multiple mating is, for any reason, already very common (rightmost arrow). Figure is modified from Kokko (1999).

Figure 6.4. Estimated adult sex ratio (ASR) based on the ratio of mean reproductive success (number of live births) for females and males for populations assigned to three mating system types. The Fisher condition applies so males and female must have the same total reproductive output. Hence any difference in mean reproductive success has to be due to a biased ASR. The data is from Brown et al (2009) who compiled data from 18 countries. Note that when Brown et al. classified a country as having two mating systems (polygyny and one other) we classified it as polygyny. Sample sizes are 6,3 and 9.