Paternal Care Decreases Foraging Activity and Body Condition,but Does Not Impose Survival Costs to Caring Males in a Neotropical Arachnid

Exclusive paternal care is the rarest form of parental investment in nature and theory predicts that the maintenance of this behavior depends on the balance between costs and benefits to males. Our goal was to assess costs of paternal care in the harvestman Iporangaia pustulosa, for which the benefits of this behavior in terms of egg survival have already been demonstrated. We evaluated energetic costs and mortality risks associated to paternal egg-guarding in the field. We quantified foraging activity of males and estimated how their body condition is influenced by the duration of the caring period. Additionally, we conducted a one-year capture-mark-recapture study and estimated apparent survival probabilities of caring and non-caring males to assess potential survival costs of paternal care. Our results indicate that caring males forage less frequently than non-caring individuals (males and females) and that their body condition deteriorates over the course of the caring period. Thus, males willing to guard eggs may provide to females a fitness-enhancing gift of cost-free care of their offspring. Caring males, however, did not show lower survival probabilities when compared to both non-caring males and females. Reduction in mortality risks as a result of remaining stationary, combined with the benefits of improving egg survival, may have played an important and previously unsuspected role favoring the evolution of paternal care. Moreover, males exhibiting paternal care could also provide an honest signal of their quality as offspring defenders, and thus female preference for caring males could be responsible for maintaining the trait.     

Anisogamy selects for male-biased care in self-consistent games with synchronous matings

We reexamine the influential parental investment hypothesis proposed by Trivers for the causal relationship between anisogamy and widespread female-biased parental care. We build self-consistent versions of Maynard Smith's simple evolutionary game between males and females over parental care, and incorporate consequences of anisogamy for gamete production and its trade-off with parental care, and for patterns of mate limitation. As male mating opportunities are limited by females, frequency-dependent selection acts on male strategies. Assuming synchrony of matings in the population, our analytical models find either symmetric sex roles or male-biased care as an evolutionarily stable strategy (ESS), in contrast to Trivers' hypothesis. We simulate evolution in asynchronously mating populations and find that diverse parental roles, including female care, can be ESS depending on the parameters. When caring males can also remate, or when females can increase the clutch size by deserting, there is stronger selection for male-biased care. Hence, we argue that the mating-caring trade-off for males is neither a necessary consequence of anisogamy nor sufficient to select for female-biased care. Instead, the factors excluded from our models—costly competitive traits, sexual selection, and partial parentage—may be necessary for the parental investment hypothesis to work.     

A model for evolution of male parental care and female multiple mating

In most animals, males gain a fitness benefit by mating with many females, whereas the number of progeny per female is unlikely to increase as a function of additional mates. Furthermore, males of internally fertilizing species run the risk of investing in offspring of other males if they provide parental care. Nevertheless, males of many avian species and a minority of mammalian species provide parental care, and females of various species mate with multiple males. I investigate a two-locus genetic model for evolution of male parental care and female multiple mating in which females gain a direct benefit by multiple mating from the paternal care they thereby elicit for their offspring. The model suggests that, first, male parental care can evolve when it strongly enhances offspring survival and the direct costs of female multiple mating (e.g., loss of energy, risk of injury, exposure to infectious diseases) are greater than its indirect benefit (e.g., acquisition of good genes, increased genetic diversity among offspring); second, female multiple mating can evolve when paternal care is important for offspring survival or the indirect benefit of multiple mating is larger than its direct cost; and, finally, male parental care and female multiple mating can co-occur.     

Multiple paternity or multiple queens: two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera

Understanding the evolution of multiple mating by females (polyandry) is an important question in behavioural ecology. Most leading explanations for polyandry by social insect queens are based upon a postulated fitness benefit from increased intracolonial genetic diversity, which also arises when colonies are headed by multiple queens (polygyny). An indirect test of the genetic diversity hypotheses is therefore provided by the relationship between polyandry and polygyny across species, which should be negative if the genetic diversity hypotheses are correct. Here, we conduct a powerful comparative investigation of the relationship between polyandry and polygyny for 241 species of eusocial Hymenoptera (ants, bees and wasps). We find a clear and significant negative relationship between polyandry and polygyny after controlling for phylogeny. These results strongly suggest that fitness benefits resulting from increased intracolonial genetic diversity have played an important role in the evolution of polyandry, and possibly polygyny, in social insects.     

Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius)

Parental care should evolve only if fitness benefits exceed fitness costs. In Cheirogaleus medius, a small nocturnal lemur of western Madagascar, we found the peculiar situation of considerable parental care by both sexes, combined with an extremely high rate of extra-pair young (EPY). In this paper, we try to elucidate the costs and benefits of parental care in C. medius, and we discuss hypotheses as to why males might actively participate in raising young, especially with regard to the high rate of EPY. The study was carried out in the dry deciduous forest of western Madagascar between 1996 and 2001. The most important components of parental care in C. medius are babysitting and guarding of the young. Observational data suggest that thermoregulatory demands during the first days after birth and defence from predators may be the driving factors selecting for this infant care behaviour. The reproducing individuals of both sexes incur considerable energetic costs by this behaviour, resulting in reduced fat stores and body condition in comparison to non-reproducing individuals. The reason why males also care for EPY remains elusive. We propose that males might not be able to detect individual relatedness and that they would jeopardise the survival of their own young if they gave no parental care. Alternatively, they might gain advantages other than direct fitness from raising EPY, for example if caring behaviour increases their chances in further reproduction, or if EPY are fathered by close kin.     

Number of males in primate groups: Comparative tests of competing hypotheses

Primate social groups frequently contain multiple males. Male group size has been hypothesized to result from male mating competition, but the selective factors responsible for the evolution of multimale groups are unclear. Short breeding seasons create situations that are not conducive for single males to monopolize mating access to females, and may therefore favor the formation of large male groups. Alternatively, since the costs of mate defense increase with the spatial clumping of females, female group size may be a primary determinant of the number of males in a primate group. We used comparative methods designed to control for the potentially confounding effects of hidden third variables associated with phylogeny to test the breeding season and female group size hypotheses for the evolution of multimale groups. Our results revealed no association between breeding season duration and the number of males in groups. In contrast, we provide support for the female group size hypothesis by demonstrating a strong pattern of correlated evolution between female and male group size. © 1996 Wiley-Liss, Inc.     

On the evolutionary pathway of parental care in mouth-brooding cichlid fishes

Evolutionary theory predicts that differences in parental care patterns among species arose from interspecific differences in the costs and benefits of care for each sex. In Galilee St Peter''s fish, Sarotherodon galilaeus (Cichlidae), male care, female care and biparental care all occur in the same population. We exploit this unusual variability to isolate conditions favouring biparental versus uniparental mouth-brooding by males or females. We first review a game-theoretic model of parental care evolution, predictions of which we test experimentally in this paper. Manipulations of the operational sex ratio show that males and females desert their offspring more frequently when the costs of care are high (in terms of lost mating opportunities). Breeding trials with males of different sizes show that small fathers desert more frequently than large fathers. We attribute this to the associated difference in the fitness benefit of biparental care relative to female-only care. Our experimental results confirm that in St Peter''s fish the probability of caring is determined facultatively according to current conditions at each spawn. The experiments and model together suggest that interspecific variation in remating opportunities and clutch size may be responsible for differences in care patterns within the sub-family Tilapiini. Our results support the hypothesis that biparental mouth-brooding was the ancestral state of both male and female uniparental mouth-brooding in cichlid fishes.     

Correlated evolution in parental care in females but not males in response to selection on paternity assurance behaviour

According to classical parental care theory males are expected to provide less parental care when offspring in a brood are less likely to be their own, but empirical evidence in support of this relationship is equivocal. Recent work predicts that social interactions between the sexes can modify co‐evolution between traits involved in mating and parental care as a result of costs associated with these social interactions (i.e. sexual conflict). In burying beetles (Nicrophorus vespilloides), we use artificial selection on a paternity assurance trait, and crosses within and between selection lines, to show that selection acting on females, not males, can drive the co‐evolution of paternity assurance traits and parental care. Males do not care more in response to selection on mating rate. Instead, patterns of parental care change as an indirect response to costs of mating for females.     

Front Cover

In most animals, competition for mating opportunities is higher among males, whereas females are more likely to provide parental care. In few species, though, these "conventional" sex roles are reversed such that females compete more strongly for matings and males provide most or all parental care. This "reversal" in sex roles is often combined with classical polyandry—a mating system in which a female forms a harem with several males. Here, we review the major hypotheses relating such role reversals to evolutionary and behavioural traits (anisogamy, phylogenetic history, sexy males, parental care, genetic paternity, trade‐off between mating and parenting, adult sex ratio) and to ecological factors (food supply, offspring predation). We evaluate each hypothesis in relation to coucals (Centropodinae), a group of nesting cuckoos of great interest for mating system and parental care theory. The black coucal (Centropus grillii) is the only known bird combining classical polyandry with altricial development of young, a costly trait with regard to parental care. Our long‐term study offers a unique possibility to compare the strongly polyandrous black coucal with a monogamous close relative breeding in the same area and habitat, the white‐browed coucal (C. superciliosus). We show that the evolution of sex roles in coucals and other animals has many different facets. Whereas phylogenetic constraints are important, confidence in genetic paternity is not. In combination with facilitating ecological conditions, adult sex ratios are key to understanding sex roles in coucals, shorebirds, and most likely also other animals. We plead for more studies including experimental tests to understand how biased adult sex ratios emerge and whether they drive sexual selection or vice versa. How do sex ratios and sexual selection interact and feedback on each other? Answers to these questions will be fundamental for understanding the evolution of sex roles in mating and parenting in coucals and other species.     

Mortality costs of sexual selection and parental care in natural populations of birds

Abstract Is the cost of reproduction different between males and females? On the one hand, males typically compete intensely for mates, thus sexual selection theory predicts higher cost of reproduction for males in species with intense male‐male competition. On the other hand, care provisioning such as incubating the eggs and raising young may also be costly, thus parental care theory predicts higher mortality for the care‐giving sex, which is often the female. We tested both hypotheses of reproductive costs using phylogenetic comparative analyses of sex‐specific adult mortality rates of 194 bird species across 41 families. First, we show that evolutionary increases in male‐male competition were associated with male‐biased mortalities. This relationship is consistent between two measures of mating competition: social mating system and testis size. Second, as predicted by the parental cost hypothesis, females have significantly higher adult mortalities (mean ± SE, 0.364 ± 0.01) than males (0.328 ± 0.01). However, the mortality cost of parental care was only detectable in males, when the influence of mating competition was statistically controlled. Taken together, our results challenge the traditional explanation of female‐biased avian mortalities, because evolutionary changes in female care were unrelated to changes in mortality bias. The interspecific variation in avian mortality bias, as we show here, is driven by males, specifically via the costs of both mating competition and parental care. We also discuss alternative hypotheses for why most birds exhibit female‐biased mortalities, whereas in mammals male‐biased mortalities predominate.     

The Evolution of Male and Female Parental Care in Fishes

In this paper we propose an explanation for (a) the predominanceof male care in fishes, and (b) the phylogenies and transitionsthat occur among care states. We also provide a general evolutionarymodel for studying the conditions under which parental careevolves. Our conclusions are as follows: (i) Parental care hasonly one benefit, the increased survivorship of young. It may,however, have three costs: a "mating cost," an "adult survivorshipcost," and a "future fertility cost." (ii) On average, malesand females will derive the same benefit from care. They probablyalso pay the same adult survivorship cost. However, their matingcost and future fertility costs may differ, (iii) A mating costusually applies only to males. However, this cost may be reducedby male territoriality and, in some situations, be entirelyremoved. Under this condition, natural selection on presentreproductive success is equivalent for males and females, (iv)When fecundity accelerates with body size in females, whilemale mating success follows a linear relationship with bodysize, future fertility costs of parental care are greater forfemales than males. Although further tests are needed, a preliminaryanalysis suggests this often may be the case in fishes. Thus,the predominance of male parental care in fishes is not explainedby males deriving greater benefits from care, but by males payingsmaller future costs. Males thus accrue a greater net fitnessadvantage from parental care (see expressions [6] and [12]).(v) The evolution of biparental care from uniparental male caremay occur because male care selects for larger egg sizes andincreased embryo investment by females. This increases the benefitto the female of parental care, (vi) By contrast, uniparentalfemale care may originate from biparental care when males areselected to desert. This occurs when female care creates a matingcost to males. In some cases male desertion may "lock" femalesinto uniparental care. However, in many other cases femalesmay be selected to desert, giving rise to "no care." (vii) Theorigin of uniparental female care from no care is rare in externallyfertilizing fishes. This is because the benefits of care rarelyoutweigh a female's future fertility costs (expression [9]).For internally fertilizing species, however, the benefit ofcare is high whereas the cost is probably low. Most of thesespecies have evolved embryo retention, (viii) When parentalcare begins with male care and moves to biparental care, ouranalysis suggests that care evolution will include cyclicaldynamics. Parental care in some fishes may thus be seen as transitionaland changing through evolutionary time rather than as an evolutionarilystable state. In theory, "no care" may be a phylogeneticallyadvanced state.     

Parental care decreases the survival of adults in the waterbug Abedus ovatus

Among animals, especially insects, care of offspring exclusively performed by males is rare. Paternal care increases survival of their offspring but may be costly for males. Our objective was to evaluate the potential survival costs of parental care in the waterbug Abedus ovatus where males only care their eggs. We conducted a capture-mark-recapture study and estimated apparent survival probabilities of parental males, non-parental males and females in a Mexican waterbug population. In addition, we also estimated recapture rates and the transition rates between non-parental males and parental males. Our results suggest that paternal care negatively affects the survival of A. ovatus since survival probability of parental males is lower than non-parental males. The recapture probability was higher in non-parental males than in parental males. The decreased probability of survival in parental males may be due to different factors. As males carry the eggs on their backs this could probably affect their swimming performance and therefore affect their ability to capture prey. Additionally, the physiological wear derived from the intense muscular activity when performing subaquatic parental care behaviors such as brood pumping, could deteriorate their condition and subsequently, their survival. Furthermore, parental males are more conspicuous to predators, especially in the later stages of egg development, which may increase mortality rates. Our results support the trade-off between current and future reproduction and provide evidence of parental care survival costs in a model system where only males care the progeny.     

Prevalence of different modes of parental care in birds

Estimates of the incidence of major classes of parental care by birds are drawn from classical studies that preceded both the publication of a massive secondary literature and the revolution driven by molecular approaches to avian phylogeny. Here, I review this literature in the light of new phylogenetic hypotheses and estimate the prevalence of six distinct modes of care: use of geothermal heat to incubate eggs, brood parasitism, male only care, female only care, biparental care and cooperative breeding. Female only care and cooperative breeding are more common than has previously been recognized, occurring in 8 and 9% of species, respectively. Biparental care by a pair-bonded male and female is the most common pattern of care but at 81% of species, the pattern is less common than once believed. I identify several problems with existing hypotheses for the evolution of parental care and highlight a number of poorly understood contrasts which, once resolved, should help elucidate avian social evolution.     

Parental antagonism and parent-offspring co-adaptation interact to shape family life

The family is an arena for conflicts between offspring, mothers and fathers that need resolving to promote the evolution of parental care and the maintenance of family life. Co-adaptation is known to contribute to the resolution of parent-offspring conflict over parental care by selecting for combinations of offspring demand and parental supply that match to maximize the fitness of family members. However, multiple paternity and differences in the level of care provided by mothers and fathers can generate antagonistic selection on offspring demand (mediated, for example, by genomic imprinting) and possibly hamper co-adaptation. While parent-offspring co-adaptation and parental antagonism are commonly considered two major processes in the evolution of family life, their co-occurrence and the evolutionary consequences of their joint action are poorly understood. Here, we demonstrate the simultaneous and entangled effects of these two processes on outcomes of family interactions, using a series of breeding experiments in the European earwig, Forficula auricularia, an insect species with uniparental female care. As predicted from parental antagonism, we show that paternally inherited effects expressed in offspring influence both maternal care and maternal investment in future reproduction. However, and as expected from the entangled effects of parental antagonism and co-adaptation, these effects critically depended on postnatal interactions with caring females and maternally inherited effects expressed in offspring. Our results demonstrate that parent-offspring co-adaptation and parental antagonism are entangled key drivers in the evolution of family life that cannot be fully understood in isolation.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

Filial cannibalism in an assassin bug

Filial cannibalism has been described in many fish species with male parental care, and has typically been explained as a response to high energetic costs of brood defence and decreased feeding opportunities during the period of care. We investigated filial cannibalism in an insect, the assassin bug Rhinocoris tristis. In this species, males guard eggs of a number of females, cannibalizing some of their offspring within the brood. We monitored guarding males in both the field and the laboratory. Males typically ate eggs around the periphery of the brood, which were those most likely to have been parasitized by wasps. However, cannibalism persisted in the laboratory in the absence of parasites, and the number of cannibalized eggs was related to the length of care and overall brood size, suggesting that males use eggs as an alternative source of food. This conclusion was further supported by the fact that males in the field did not lose weight while guarding, despite being unable to forage efficiently while caring. Males were also observed to adopt broods, but in a laboratory experiment did not eat more eggs from adopted than from their own broods.     

Short-term benefits,but transgenerational costs of maternal loss in an insect with facultative maternal care

A lack of parental care is generally assumed to entail substantial fitness costs for offspring that ultimately select for the maintenance of family life across generations. However, it is unknown whether these costs arise when parental care is facultative, thus questioning their fundamental importance in the early evolution of family life. Here, we investigated the short-term, long-term and transgenerational effects of maternal loss in the European earwig Forficula auricularia, an insect with facultative post-hatching maternal care. We showed that maternal loss did not influence the developmental time and survival rate of juveniles, but surprisingly yielded adults of larger body and forceps size, two traits associated with fitness benefits. In a cross-breeding/cross-fostering experiment, we then demonstrated that maternal loss impaired the expression of maternal care in adult offspring. Interestingly, the resulting transgenerational costs were not only mediated by the early-life experience of tending mothers, but also by inherited, parent-of-origin-specific effects expressed in juveniles. Orphaned females abandoned their juveniles for longer and fed them less than maternally-tended females, while foster mothers defended juveniles of orphaned females less well than juveniles of maternally-tended females. Overall, these findings reveal the key importance of transgenerational effects in the early evolution of family life.     

Protandrous arrival timing to breeding areas: a review

Protandry, the earlier arrival of males to breeding areas than females, is a common pattern of sex-biased timing in many animal taxa (e.g. some insects, fish, amphibians, reptiles, birds and mammals). The adaptive significance of protandry is not fully understood and, since the 1970s, at least seven hypotheses for protandry have been proposed. We describe each of these hypotheses and summarize what is known about each. In three of these hypotheses, the relative arrival timing of males and females has no direct fitness consequences for males or females, but selection for different timing in each sex indirectly produces protandry. In the other four hypotheses, the difference between male and female timing has fitness consequences for males or females and selection directly maintains the fitness-maximizing degree of sex-biased timing. The hypotheses are not mutually exclusive, and the degree of multiple mating by males and the occurrence of male territoriality seem to determine the relative importance of each hypothesis. In order to understand the adaptive significance of sex-biased timing, future studies need to consider all the alternatives and to assess the costs and benefits to males of early arrival relative to calendar date, to other males and to females.     

The evolution of avian parental care

A stage model traces key behavioural tactics and life-history traits that are involved in the transition from promiscuity with no parental care, the mating system that typifies reptiles, to that typical of most birds, social monogamy with biparental care. In stage I, females assumed increasing parental investment in precocial young, female choice of mates increased, female-biased mating dispersal evolved and population sex ratios became male biased. In stage II, consortships between mating partners allowed males to attract rare social mates, provided a mechanism for paternity assessment and increased female ability to assess mate quality. In stage III, relative female scarcity enabled females to demand parental investment contributions from males having some paternity certainty. This innovation was facilitated by the nature of avian parental care; i.e. most care-giving activities can be adopted in small units. Moreover, the initial cost of care giving to males was small compared with its benefit to females. Males, however, tended to decline to assume non-partitionable, risky, or relatively costly parental activities. In stage IV, altriciality coevolved with increasing biparental care, resulting in social monogamy. Approaches for testing behavioural hypotheses are suggested.     

The evolution of paternal care with overlapping broods

Most attempts to model the evolution of parental care assume that caring and mating are mutually exclusive activities (i.e., individuals acquire and guard broods "sequentially"). However, in most fish and certain insects, males can keep mating and collecting additional eggs while continuing to guard broods obtained earlier (i.e., males guard "overlapping" broods). We present a model of parental care with overlapping broods in which males can mate and guard simultaneously, even though there is a trade-off between these two activities. Within this framework, we show that male care is favored by short female processing times and high population densities, which minimize the mating cost of care. Relatively low mortality while guarding is also important for the stability of male care. Female care, on the other hand, is favored by long female processing times and low populations densities, which lead to longer intermating intervals. Biparental care is stable only when the cost to benefit ratio of care was not biased toward either sex. We derive quantitative estimates of fitness for different strategies for two species of assassin bugs with male and female uniparental care and show that the model predicts the correct form of care for both species. We believe our model might help explain the prevalence of male uniparental care in certain taxa, such as fish.