When fathers make the difference: efficacy of male sexually selected antimicrobial glands in enhancing fish hatching success

1.  Egg and offspring resistance to pathogens is a major determinant of survival and has been mainly ascribed to maternal factors. However, paternal production of antimicrobials was recently suggested to increase offspring survival in species where males perform egg care.
2.  In the peacock blenny, Salaria pavo , a demersal spawning species where males exhibit a pair of anal glands producing lysozyme-like compounds, we tested the antimicrobial activity and the egg protection efficacy of these glands. The anal gland secretion (AGS) has an inhibitory effect on the growth of both Gram-negative and Gram-positive bacteria, including those causing the most severe fish diseases in marine culture. The egg clutches cared for by males deprived of anal glands have a significantly lower survival rate than those cared for by sham-operated males and non-viable eggs showed clear signs of bacterial infection.
3.  Anal gland secretion production and its protein content are proportional to gland size. In species where male parental care plays a crucial role in offspring survival, females are expected to assess mates selecting those traits that are reliably associated with parental ability. Hence, we experimentally challenged females with dummy males differing in anal gland size. Females definitely preferred dummy males with larger anal glands, suggesting that their choice is driven by the pursuit of direct fecundity benefits.
4.  These findings indicate that antimicrobial production is a crucial component of male parental care. The contribution of antimicrobials to male performance as fathers suggests that the development of traits devoted to this function may influence male attractiveness and be sexually selected.     

Contrasting Parental Tasks Influence Parental Roles for Paired and Single Biparental Cichlid Fish

Biparental care of young occurs when both parents provide some sort of care for offspring and can include a wide variety of behaviors, yet often studies focus on single aspects of parental care when trying to determine how each parent contributes. Here, we presented the biparental convict cichlid fish (Amatitlania nigrofasciata) with two conflicting parental behaviors: retrieval of non‐swimming offspring that have been displaced from the nest and defense against a conspecific intruder, a potential brood predator. We examined single males, single females, and pairs of parents to determine how males and females each contributed to overall parental care. Traditionally in this species, parents exhibit a division of labor (in which each parent contributes to all parental activities), but also exhibit a division of roles (in which males tend to favor the role of defense and females tend to favor more direct care, spending more time with offspring). We hypothesized that single parents would compensate for their absent mate, but that males and females would still favor preferred roles. Additionally, we hypothesized that there would be an asymmetrical expansion of roles, with females being more flexible. Our results show that the preferred roles of both parents were evident even when parents were without their mates and that males and females differed in their compensatory levels, at least when compared to the behaviors of the intact pair. Contrary to our prediction, females seem unable to fully compensate for the defensive behaviors usually exhibited by males, while males shifted completely to retrieve displaced offspring.     

Paternity analysis in the golden egg bug using AFLPs: do the males preferentially accept their true genetic offspring?

Abstract.  1. The evolution of parental care and intraspecific parasitism involve conflicts of interest between mothers and other potential care givers who contribute to enhance offspring survival. In the golden egg bug, Phyllomorpha laciniata Villers (Heteroptera: Coreidae), females lay eggs on conspecifics and on plants. The adaptive significance of egg carrying in this species has been the subject of some controversy, which can only be resolved by determining the genetic relationship between the eggs and the adult who carries them. This study examined whether male acceptance of true genetic offspring occurs with a higher frequency than that expected from random oviposition on conspecifics.
2. Paternity analysis, using Amplified Fragment Length Polymorphism (AFLP) markers, was conducted on eggs carried by males housed with field-mated females.
3. Out of the total number of eggs sired by males in the experimental groups, the proportion of eggs carried by males that were their true genetic offspring was 30.8%.
4. Monte Carlo methods show that the probability of a male accepting an egg that is his true genetic offspring is higher than expected if females dumped eggs on males at random.
5. These results suggest that paternal care plays an important role in the maintenance of male egg carrying in this species. In addition, the methodology developed may become useful in determining true genetic parents in other species in which neither the father nor the mother can be determined by observational methods.     

The frequency and fitness consequences of communal breeding in a natural population of burying beetles: a test of reproductive skew

Abstract.  1. Reproductive cooperation occurs in diverse taxa and a defining characteristic of these social systems is how reproduction is shared. Both male and female burying beetles ( Nicrophorus spp.) facultatively form associations to bury a carcass and rear a single brood, making burying beetles a model system for testing skew theory.
2. In this study, 50% of 40–45 g carcasses and 75% of 55–60 g ones were buried by more than one male and/or female Nicrophorus tomentosus .
3. Females were significantly more likely to cooperate on 55–60 g carcasses than on 40–45 g ones.
4. Analysis of parentage of 13 broods using microsatellite loci as genetic markers showed that maternity analysis of only 2% of the young excluded all females captured leaving the brood chamber after burial. Males previously mated with resident females or displaced by resident males fathered 7% of the young.
5. The male and female remaining the longest were usually the parents of the most offspring, and reproductively dominant individuals also tended to be the largest.
6. Although all but two or three individuals that helped to bury the carcass produced some offspring, reproduction was often not shared equitably. Reproduction of females was significantly skewed on six of nine 40–45 g carcasses but shared fairly equitably on all three 55–60 g ones. Reproduction was skewed among males on 7 of 10 broods.
7. Both males and females relinquished a greater proportion of the brood as the days of assistance from all consexuals increased.     

Intraspecific female brood parasitism in the dung beetle Onthophagus taurus

Abstract.  1. Brood parasitism occurs when individuals parasitise each others' investment into parental care, and has been documented primarily as an interspecific interaction. Intraspecific brood parasitism, in contrast, is often difficult to detect and quantify, and evidence for it is comparatively scarce. The present study documents the occurrence of intraspecific brood parasitism by females of the tunnelling dung beetle Onthophagus taurus , and investigates the contributions of two variables to the propensity of female brood parasitism: female body size and dung desiccation rate.
2. Female O. taurus were found to routinely utilise brood balls made by conspecific females as food provisions for their own offspring.
3. Contrary to expectations, large and small females did not differ in the likelihood of engaging in brood-parasitic behaviour.
4. Dung desiccation rate appeared to influence likelihood of brood parasitism. Females that were given access to rapidly drying dung were significantly more likely to detect and utilise brood balls produced by conspecific females.
5. While interspecific brood parasitism has been documented in dung beetles before, the present study is among the first to present evidence for intraspecific brood parasitism as an alternative reproductive tactic of female dung beetles. Results are discussed in the context of the evolutionary ecology of onthophagine beetles.     

Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus

Abstract.— Parents often have important influences on the development of traits in their offspring. One mechanism by which parents are able to influence offspring phenotype is through the level of care they provide. In onthophagine dung beetles, parents typically provision their offspring by packing dung fragments into a brood mass. Onthophagus taurus males can be separated into two discrete morphs: Large, "major" males have head horns, whereas "minor" males are hornless. Here we show that a switch in parental provisioning strategies adopted by males coincides with the switch in male morphology. Male provisioning results in the production of heavier brood masses than females will produce alone. However, unlike females in which the level of provisioning increases with body size in a continuous manner, the level of provisioning provided by males represents an "all-or-none" tactic with all major males providing a fixed level of provisioning irrespective of their body size. Offspring size is determined largely by the quantity of dung provided to the developing larvae so that paternal and maternal provisioning affects the body size and horn size of offspring produced. The levels of provisioning by individual parents are significantly repeatable, suggesting paternal and maternal effects as candidate indirect genetic effects in the evolution of horn size in the genus Onthophagus .     

Sex differences in biparental care as offspring develop: a field study of convict cichlids (<Emphasis Type="Italic">Amatitlania siquia</Emphasis>)

Parental investment theory states that parents should contribute more to older offspring. Differences between the sexes also influence how each parent contributes to offspring in biparental species. Here, we examined a naturally occurring population of biparental convict cichlids in Costa Rica to determine how each parent cared for offspring during two distinct offspring development stages. Consistent with the predictions of the reproductive value hypothesis, we hypothesized that the levels of parental contribution would be relative to the value that each parent places on a brood. We predicted that female parents would contribute more than male parents because female convict cichlids have lower future reproductive success than males. Additionally, we predicted that both parents should contribute more to older offspring, either due to the young’s increased susceptibility to predation (i.e., the vulnerability hypothesis) or because of the longer period of time parents have been interacting with older offspring (i.e., feedback hypotheses). This increase in investment by males should coincide with a change in the coordination of care between parents. Detailed observations of parental pairs in their natural habitat supported these predictions. Females contributed more to broods than males and were relatively unaffected by offspring age while males spent significantly more time with older, free-swimming fry. Additionally, males tended to leave younger offspring more than females did, and were more likely to do so consecutively with younger offspring. This suggests that the coordination of duties between parents changes as parental investment changes. Overall, these data support both the reproductive value and the vulnerability hypotheses, but not necessarily the feedback hypothesis.     

Differential response by males and females to manipulation of partner contribution in the great tit (Parus major)

1.  In birds with bi-parental care, handicapping is often assumed to decrease the amount of parental care of the handicapped partner. We discuss how handicapping could alter the shape of the handicapped bird's survival–effort curve (theoretical curve relating the survival of a parent to its effort) and show that the optimal response could yield a decrease, no response or even an increase in effort of the handicapped bird.
2.  Male or female great tits Parus major (L.) were handicapped during the nestling period by clipping a number of feathers in order to study the effects on parental care and body condition.
3.  Handicapped males significantly decreased their feeding rates, while handicapped females did not. Condition of handicapped females significantly deteriorated, while condition of handicapped males did not change during the experiment. Females with a handicapped partner fully compensated for their partner's decrease in work rate, while males with a handicapped partner did not show any compensation and even tended to decrease their feeding rates.
4.  Using an inverse optimality approach, we reconstructed the theoretical curve relating the survival of a parent to its effort on the basis of the experimental effects. The handicapped male's survival–effort curve appeared to be slightly steeper than that of handicapped females. This suggests that handicapped males suffer more from an increase in effort than handicapped females.     

Male age mediates reproductive investment and response to paternity assurance

Theory predicts that male response to reduced paternity will depend on male state and interactions between the sexes. If there is little chance of reproducing again, then males should invest heavily in current offspring, regardless of their share in paternity. We tested this by manipulating male age and paternity assurance in the burying beetle Nicrophorus vespilloides. We found older males invested more in both mating effort and parental effort than younger males. Furthermore, male age, a component of male state, mediated male response to perceived paternity. Older males provided more prenatal care, whereas younger males provided less prenatal care, when perceived paternity was low. Adjustments in male care, however, did not influence selection acting indirectly on parents, through offspring performance. This is because females adjusted their care in response to the age of their partner, providing less care when paired with older males than younger males. As a result offspring, performance did not differ between treatments. Our study shows, for the first time, that a male state variable is an important modifier of paternity–parental care trade-offs and highlights the importance of social interactions between males and females during care in determining male response to perceived paternity.     

Parental care influences social immunity in burying beetle larvae

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How Similar is the Coordination of Parental Roles Among Different Pairs? An Examination of a Monogamous Fish

Although most studies on biparental care assume that parents cooperate in raising offspring, few studies have documented how parents coordinate their activities. Using the biparental convict cichlid (Archocentrus nigrofasciatum) we compared the parental behavior of both single (‘widowed’) parents and individuals within pairs during the 5 d when the offspring were in the relatively uniform and stationary wriggler stage. In particular, we were interested in the consistency of day‐to‐day parental activities among single individuals and among individuals within pairs. Single parents showed differences in most parental activities that were consistent from one day to the next. This day‐to‐day consistency remained after an intruder was added and / or the mate was present. Thus, although the social context changed (i.e., presence or absence of mate, presence or absence of an intruder), an individual's consistency remained. The male and female within pairs were significantly correlated in the time spent on most parental activities across experimental pairs. Thus, while individuals within pairs were unique in their performance of a parental activity, paired males and females managed a high degree of correlation (i.e., coordination). In general, pairs were homogeneous in the degree to which males and females were correlated across different parental activities.     

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.     

Interactions among intraspecific competition, emergence patterns, and host selection behaviour in Ips pini (Coleoptera: Scolytinae)

Abstract.  1. Variations in developmental conditions of bark beetles, particularly intraspecific competition, can induce morphological and physiological modifications in the offspring. It is hypothesised that intraspecific competition could also affect host selection behaviour. Such behavioural changes might be manifested in response to host (alpha-pinene) or beetle (verbenone) compounds.
2.  Ips pini were bred at different densities. The offspring were measured for size, weight, and lipid concentration, and then subjected to tunnelling bioassays in agar media amended with varying amounts of alpha-pinene or verbenone.
3. High parental colonisation densities reduced emergence time of parents and offspring. Increasing colonisation density and emergence time had a negative influence on offspring vigour, resulting in a reduction of the distance tunnelled by the beetles.
4. Both alpha-pinene and verbenone were repellent. Surprisingly, verbenone was also toxic at high concentrations, with its effect being greater on beetles arising from high densities. The repellent effect of these compounds did not vary according to colonisation density, but for both compounds, at a 1.5 mg g^–1 concentration, it increased with emergence time.
5. The consequences of varying vigour and behaviour in relation to developmental conditions and emergence patterns on population dynamics of I. pini are discussed.     

Sex Differences in Retrieval Behavior by the Biparental Convict Cichlid

Biparental species occasionally demonstrate a division of roles in which parents perform sex-typical tasks, with females offering direct care and spending the majority of their time with the offspring while males are more indirect in their care, providing the majority of defense against potential brood predators. To examine the flexibility in the sex-typical roles shown by convict cichlids ( Amatitlania nigrofasciata ), we displaced non-swimming young at three different distances from the nest and then analyzed the retrieval behaviors of each parent. Retrieval of altricial young is a behavior commonly used to measure parental care in mammalian studies, but has rarely been used in other taxa. We found sex differences in retrieval behavior: on average, females retrieved young close to the nest and males retrieved young far from the nest. This difference in parental contribution suggests a division of labor with sex-specific roles. Sex differences may be due to proximity to young and/or apparent risk of offspring predation. Additionally, we found that latency to first retrieval and total time spent retrieving young remained consistent across the various displacement distances, suggesting that retrieval is an essential parental behavior. Additionally, we include observations of wriggler retrieval by parents in a natural population of Costa Rican convict cichlids.     

The Effect of Female Condition on Maternal Care in the European Earwig

Parental care typically enhances offspring fitness at costs for tending parents. Asymmetries in genetic relatedness entail potential conflicts between parents and offspring over the duration and the amount of care. To understand how these conflicts are resolved evolutionarily, it is important to understand how individual condition affects offspring and parental behaviour and whether parents or offspring make active choices in their interactions. Condition effects on offspring have been broadly studied, but the effect of parental condition on parent–offspring interactions is less well understood, in particular in species where care is facultative and offspring have the option to beg for food from the parents or to self‐forage. In this study, we carried out two experiments in the European earwig Forficula auricularia, a system where females provide facultative care, in which we manipulated female condition (through a high‐food and low‐food treatment) and the degree by which mothers and offspring could make active choices. In a first experiment, where female mobility was limited, female condition had no significant effect on the rate of offspring self‐foraging, which increased with nymph age. In a second experiment, nymph access to food was limited and females in poor nutritional condition provided food to significantly fewer nymphs than high condition females. In both experiments, offspring attendance remained at a constantly high level and was independent of female condition even after experimental separation of females and offspring. Our results show that earwig nymphs do not use cues of female condition to adjust rates of self‐foraging, that females control food provisioning depending on their own condition, and that females and nymphs share control over offspring attendance, a form of care not influenced by female condition.     

A female's past experience with predators affects male courtship and the care her offspring will receive from their father

Differential allocation occurs when individuals adjust their reproductive investment based on their partner''s traits. However, it remains unknown whether animals differentially allocate based on their partner''s past experiences with predation risk. If animals can detect a potential mate''s experience with predators, this might inform them about the stress level of their potential mate, the likelihood of parental effects in offspring and/or the dangers present in the environment. Using threespined stickleback (Gasterosteus aculeatus), we examined whether a female''s previous experience with being chased by a model predator while yolking eggs affects male mating effort and offspring care. Males displayed fewer conspicuous courtship behaviours towards females that had experienced predation risk in the past compared with unexposed females. This differential allocation extended to how males cared for the resulting offspring of these matings: fathers provided less parental care to offspring of females that had experienced predation risk in the past. Our results show for the first time, to our knowledge, that variation among females in their predator encounters can contribute to behavioural variation among males in courtship and parental care, even when males themselves do not encounter a predator. These results, together with previous findings, suggest that maternal predator exposure can influence offspring development both directly and indirectly, through how it affects father care.     

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.     

Differences in Patterns of Reproductive Allocation between the Sexes in Nicrophorus orbicollis

Organisms are selected to maximize lifetime reproductive success by balancing the costs of current reproduction with costs to future survival and fecundity. Males and females typically face different reproductive costs, which makes comparisons of their reproductive strategies difficult. Burying beetles provide a unique system that allows us to compare the costs of reproduction between the sexes because males and females are capable of raising offspring together or alone and carcass preparation and offspring care represent the majority of reproductive costs for both sexes. Because both sexes perform the same functions of carcass preparation and offspring care, we predict that they would experience similar costs and have similar life history patterns. In this study we assess the cost of reproduction in male Nicrophorus orbicollis and compare to patterns observed in females. We compare the reproductive strategies of single males and females that provided pre- and post-hatching parental care. There is a cost to reproduction for both males and females, but the sexes respond to these costs differently. Females match brood size with carcass size, and thus maximize the lifetime number of offspring on a given size carcass. Males cull proportionately more offspring on all carcass sizes, and thus have a lower lifetime number of offspring compared to females. Females exhibit an adaptive reproductive strategy based on resource availability, but male reproductive strategies are not adaptive in relation to resource availability.     

Fighting, dispersing, and sneaking: body-size dependent mating tactics by male Librodor japonicus beetles

Abstract.  1. Scaling relations between weapons and body size depart from linearity in many male beetles. In many previous studies, these males have been divided into major and minor males with a switch point, that is male dimorphism. Major and minor males adopt strikingly different reproductive tactics.
2. We found three size-dependent behaviours, i.e. fighting, dispersing, and sneaking, however, among Librodor japonicus males with dimorphic mandibles. We statistically classified males into large, medium, and small (L-, M-, and S-males) sizes and then compared the dispersal of males from a foraging site, behaviours to gain access to females, and sizes of mandibles, wings, and testes.
3. M-males dispersed earlier than L- and S-males from a territory in a field, but no difference in the frequency of dispersal was observed between L- and S-males. Observations of male–male interactions in the laboratory showed that L-males frequently fought with other males in a fighting arena, while S-males often showed sneaking behaviour without fighting.
4. On the basis of the morphological analysis, we concluded that S-males invested their available resources more in sperm (= testes), M-males more in wings, and L-males more in mandibles in L. japonicus .
5. Even though a morphological male dimorphism was detected, it might be possible to classify the males of the armed beetles into more than two behavioural tactics if we examine their behaviours.