Sexual selection determines parental care patterns in cichlid fishes

Despite a massive research effort, our understanding of why, in most vertebrates, males compete for mates and females care for offspring remains incomplete. Two alternative hypotheses have been proposed to explain the direction of causality between parental care and sexual selection. Traditionally, sexual selection has been explained as a consequence of relative parental investment, where the sex investing less will compete for the sex investing more. However, a more recent model suggests that parental care patterns result from sexual selection acting on one sex favoring mating competition and lower parental investment. Using species-level comparative analyses on Tanganyikan cichlid fishes we tested these alternative hypotheses employing a proxy of sexual selection based on mating system, sexual dichromatism, and dimorphism data. First, while controlling for female reproductive investment, we found that species with intense sexual selection were associated with female-only care whereas species with moderate sexual selection were associated with biparental care. Second, using contingency analyses, we found that, contrary to the traditional view, evolutionary changes in parental care type are dependent on the intensity of sexual selection. Hence, our results support the hypothesis that sexual selection determines parental care patterns in Tanganyikan cichlid fishes.     

Parental effort and reproductive skew in coalitions of brood rearing female common eiders

Members of breeding groups face conflicts over parental effort when balancing antipredatory vigilance and feeding. Empirical evidence has shown disparate responses to manipulations of parental effort. We develop a model in which we determine the evolutionarily stable effort of partners given their body conditions, allowing the benefits of shared care to be unevenly divided, and we test this model's predictions with data on common eiders (Somateria mollissima). Eiders show uniparental female care; females may share brood rearing, or they may tend alone, and their body condition at hatching of the young shows large environmentally induced variation. The model predicts that parental effort (vigilance) in a coalition is lower than when tending alone, controlling for parental condition; this prediction is supported by the data. The parental effort in a coalition should be positively correlated with body condition, and this prediction is also supported. Finally, parental effort should increase when partner condition decreases and vice versa; this prediction is partially supported. The Nash bargaining game may provide promising avenues by which to determine the precise settlement of reproductive skew and effort between coalition partners in the future.     

Paternal Care by Genetic Fathers and Stepfathers II: Reports by Xhosa High School Students

In this article we present a biosocial model of human male parental care that allows relationship (mating) effort to influence male parental allocations. The model recognizes four classes of relationships between men and the children they parent: genetic offspring of current mates (combined relationship and parental effort), genetic offspring of previous mates (parental effort solely), step offspring of current mates (relationship effort solely), and stepchildren of previous mates (essentially no expected investment). We test the model using data on parental investment collected from 340 Xhosa high school students in Cape Town, South Africa. Six measures of paternal investment are examined: the amount of money men spent on students for school, clothing, and miscellaneous expenditures, respectively, and how often men spent time with children, helped them with their homework, or spoke English with them. The tests provide support for the roles of both parental and relationship effort in influencing parental care: men invest significantly more in their genetic offspring and in the children of their current mates. We also examine several proximate influences on parental care, specifically the age and sex of the child, and the percentage of the child's life the father figure coresided with him or her.     

Parental and Mating Effort: Is There Necessarily a Trade‐Off?

One of the common assumptions in the study of the evolution of parental care is that trade-offs exist between parental investment and other fitness-related traits. In general, this body of work follows the traditional definition that parental investment (in the current offspring) decreases that individual's ability to invest in future reproduction ( Trivers 1972 ). However, examination of the empirical evidence shows that assuming a trade-off between parental and mating effort is not always appropriate. This overemphasis on a trade-off between mating and parental effort has arisen in part because of an oversimplification of female reproductive strategies, a failure to consider interactions between the sexes, and a tendency to consider behaviours as unifunctional, thereby ignoring the more complex relationship between mating and parental effort in many species. Here, we first examine the empirical evidence for trade-offs between mating and parental effort in males and females to ask when trade-offs occur and what pattern they take. By highlighting a number of exemplar species, we then explore how the presence or absence of trade-offs relates to mate choice and sexual selection in both sexes. Finally, we highlight the importance of considering individual variation, which has been particularly overlooked in examinations of female investment, and how preferences in one sex may influence the existence and our interpretation of apparent trade-offs in the other sex.     

Tri-axial accelerometry shows differences in energy expenditure and parental effort throughout the breeding season in long-lived raptors

Cutting-edge technologies are extremely useful to develop new workflows in studying ecological data, particularly to understand animal behavior and movement trajectories at the individual level. Although parental care is a well-studied phenomenon, most studies have been focused on direct observational or video recording data, as well as experimental manipulation. Therefore, what happens out of our sight still remains unknown. Using high-frequency GPS/GSM dataloggers and tri-axial accelerometers we monitored 25 Bonelli’s eagles Aquila fasciata during the breeding season to understand parental activities from a broader perspective. We used recursive data, measured as number of visits and residence time, to reveal nest attendance patterns of biparental care with role specialization between sexes. Accelerometry data interpreted as the overall dynamic body acceleration, a proxy of energy expenditure, showed strong differences in parental effort throughout the breeding season and between sexes. Thereby, males increased substantially their energetic requirements, due to the increased workload, while females spent most of the time on the nest. Furthermore, during critical phases of the breeding season, a low percentage of suitable hunting spots in eagles’ territories led them to increase their ranging behavior in order to find food, with important consequences in energy consumption and mortality risk. Our results highlight the crucial role of males in raptor species exhibiting biparental care. Finally, we exemplify how biologging technologies are an adequate and objective method to study parental care in raptors as well as to get deeper insight into breeding ecology of birds in general.     

Song as an indicator of male parental effort in the sedge warbler

Repertoire size has been found to be a sexually selected trait in a number of bird species, although the advantages of mating with a male who possesses a complex song remain unclear. We studied the potential role of song as an indicator of male parental effort in the sedge warbler Acrocephalus schoenobaenus. The male provisioning rate was used as a measure of male parental effort and was found to increase with nestling age and brood size. When controlling for chick age, brood size and other variables, we found a highly significant positive correlation between a measure of song complexity (repertoire size) and male parental effort. Both male parental effort and repertoire size were found to be positively correlated with chick weight when controlling for chick age. We found no correlation between a measure of song output (amount of song flighting) or territory size and parental effort. Repertoire size is known to be the most important cue in female choice amongst sedge warblers and we discuss the possible reasons for this. We suggest that, in choosing a male with a large repertoire, a female obtains not only indirect benefits but also direct benefits in the form of increased parental effort.     

The costs of parental care: a meta-analysis of the trade-off between parental effort and survival in birds

A fundamental premise of life-history theory is that organisms that increase current reproductive investment suffer increased mortality. Possibly the most studied life-history phenotypic relationship is the trade-off between parental effort and survival. However, evidence supporting this trade-off is equivocal. Here, we conducted a meta-analysis to test the generality of this tenet. Using experimental studies that manipulated parental effort in birds, we show that (i) the effect of parental effort on survival was similar across species regardless of phylogeny; (ii) individuals that experienced reduced parental effort had similar survival probabilities than control individuals, regardless of sex; and (iii) males that experienced increased parental effort were less likely to survive than control males, whereas females that experienced increased effort were just as likely to survive as control females. Our results suggest that the trade-off between parental effort and survival is more complex than previously assumed. Finally, our study provides recommendations of unexplored avenues of future research into life-history trade-offs.     

Paternity and paternal effort in the pumpkinseed sunfish

Theoretical models suggest that males should adjust their parentaleffort according to paternity when parental effort is costly,paternity varies among clutches, and males have a cue to assesspaternity. To date, nearly all tests of this theory have beenconducted using birds as model organisms. In this study we examinedthese three factors and the relationship between paternity andmale parental care in a fish system. In the pumpkinseed sunfish(Lepomis gibbosus), parental care is provided exclusively bymales (parentals), but some males (sneakers) parasitize othersby sneaking fertilizations. Parental males significantly lostweight during the parental care period. Clutch size and amountof parental effort did not affect a male's probability of obtainingmore eggs. Paternity was variable among broods. The proportionof young sired by a parental male was not associated with frequencyof fanning eggs or defense of hatched young, but was positivelycorrelated with levels of nest defense during the egg stage.Egg survivorship might restrict an adjustment of fanning behavior,and a general decline in parental behavior (with brood age)might explain the lack of adjustment once the eggs hatch. Parentalmales did not adjust their care when we experimentally manipulatedone possible cue of paternity. Together, these results indicatethat male pumpkinseeds do adjust their care in relation to paternity,but the cues used to assess paternity are not clear.     

Variation in parental rearing expenditure triggers short‐term physiological effects on offspring in a long‐lived seabird

Parental care in long‐lived bird species involves a trade‐off between the benefits of increasing the effort expended on current offspring and the costs that this represents for future reproductive output. Under regimes of high environmental variability, long‐lived seabirds can adjust their breeding effort to buffer the negative effects of this variability on their offspring. However, the potential impacts of variation in breeding effort on offspring physiology in the short term and on longer‐term survival are poorly understood. In this study, we manipulated brood age through a cross‐fostering experiment to assess whether increasing or decreasing parental reproductive expenditure led to costs in Blue‐footed Booby Sula nebouxii chicks. Specifically, we tested the consequences of altered parental reproductive expenditure on the offspring's physiological condition (plasma metabolites, heterophil to lymphocyte ratio (H/L) and body condition index (BCI)) and survival. Offspring from broods in which parental investment was experimentally increased showed a lower BCI and lower alkaline phosphatase levels and higher H/L ratios than controls. Conversely, offspring showed the opposite pattern when reproductive expenditure was experimentally decreased. We observed no effects of manipulation of parental investment on triglyceride levels or on survival rates. Although our findings suggest that Blue‐footed Booby parents have the ability to adjust their breeding effort according to the demands of their offspring, parental effort could influence the effect of hatching order by suppressing the aggressive tendency of the senior chick.     

Energetics of parental care in six syntopic centrarchid fishes

We studied parental behavior in six syntopically breeding species of centrarchid fishes to determine whether energetic costs could contribute to our understanding of the diversity of parental care. We used a combination of underwater videography, radio telemetry and direct observation to examine how the cost of parental care varied with both its duration and intensity. Duration of parental care, activity patterns, and energetic costs varied widely among species. Overall, the duration of care increased with parental size between species. When energetic costs were adjusted for species-specific differences in the duration of parental care, the cost of parental care also increased with mean size of the species. Species with extended parental care exhibited stage-specific patterns of activity and energy expenditure consistent with parental investment theory, whereas fish with short duration parental care tended to maintain high levels of activity throughout the entire period of parental care. The only apparent exception (a species with brief parental care but stage-specific behavior) was a species with multiple breeding bouts, and thus effectively having protracted parental care. These data suggest that some species with short duration parental care can afford not to adjust parental investment over stages of offspring development. Using our empirical data on parental care duration and costs, we reevaluated the relationship between egg size and quality of parental care. Variation in egg size explained almost all of the observed variation in total energetic cost of parental care, and to a lesser degree, duration—the larger the eggs, the more costly the parental care. This research highlights the value of incorporating energetic information into the study of parental care behavior and testing of ecological theory.     

Have your cake and eat it too: male sand gobies show more parental care in the presence of female partners

Traditionally, male parental effort and mate attraction effortare expected to be in conflict as they compete for the sameresource budget. However, the quality of care provided by themale may be of a direct benefit to females and may provide animportant mate choice cue. In a laboratory experiment, we examinedhow males modified their parental behavior with respect to matingopportunity by allowing male sand gobies to mate with a singlefemale either in a big or small nest (a constraint on futuremating potential). We then exposed half of these males to thevisual stimulus from additional females and recorded male eggfanning and nest building (two components of care), courtshipbehavior, and reproductive success through out the brood cycle.We found that males fanned longer and more frequently and didmore nest construction in the presence of females and in bignests. Males guarding large nests courted females more thandid males guarding small nests. All males consumed eggs duringthe brood cycle, but complete clutch cannibalism was most frequentwhen males were guarding small nests in the absence of females.The pattern of filial cannibalism that we observed suggeststhat males prematurely terminated care when their reproductivepotential was low, that is, when there was little nest spacefor additional mating and no mates present. We found no supportfor a trade-off between mate attraction and parental care. Indeed,taken together our results suggest that males may use parentalcare as a courtship strategy and that males who invest in mateattraction also have higher parental effort.     

Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem‐defending arachnid

When there is a temporal trade‐off between mating effort and parental care, theoretical models predict that intense sexual selection on males leads to reduced paternal care. Thus, high‐quality males should invest more in mating effort because they have higher chances of acquiring mates, whereas low‐quality males should bias their investment towards parental care. Once paternal care has evolved, offspring value should also influence males’ decisions to invest in offspring attendance. Here, we performed a manipulation under field conditions to investigate the factors that influence male allocation in either mating effort or parental care. We predicted that facultative paternal care in the harem‐holding harvestman Serracutisoma proximum would be negatively influenced by male attractiveness and positively influenced by offspring value. We found that attractive males were less likely to engage in egg attendance and that the higher the perceived paternity, the higher the caring frequency. Finally, egg mortality was not related to caring frequency by males, but predation pressure was much lower than that recorded in previous studies with the same population. Thus, the benefits of facultative male care may be conditional to temporal variation in the intensity of egg predation. In conclusion, males adjust their investment in either territory defence or egg attendance according to their recent mating history and perceived paternity. Our findings suggest that exclusive paternal care can evolve from facultative paternal care only if the trade‐off between mating effort and parental care is circumvented.     

Corticosterone predicts foraging behavior and parental care in macaroni penguins

Corticosterone has received considerable attention as the principal hormonal mediator of allostasis or physiological stress in wild animals. More recently, it has also been implicated in the regulation of parental care in breeding birds, particularly with respect to individual variation in foraging behavior and provisioning effort. There is also evidence that prolactin can work either inversely or additively with corticosterone to achieve this. Here we test the hypothesis that endogenous corticosterone plays a key physiological role in the control of foraging behavior and parental care, using a combination of exogenous corticosterone treatment, time-depth telemetry, and physiological sampling of female macaroni penguins (Eudyptes chrysolophus) during the brood-guard period of chick rearing, while simultaneously monitoring patterns of prolactin secretion. Plasma corticosterone levels were significantly higher in females given exogenous implants relative to those receiving sham implants. Increased corticosterone levels were associated with significantly higher levels of foraging and diving activity and greater mass gain in implanted females. Elevated plasma corticosterone was also associated with an apparent fitness benefit in the form of increased chick mass. Plasma prolactin levels did not correlate with corticosterone levels at any time, nor was prolactin correlated with any measure of foraging behavior or parental care. Our results provide support for the corticosterone-adaptation hypothesis, which predicts that higher corticosterone levels support increased foraging activity and parental effort.     

A cost of maternal care in the dung beetle Onthophagus taurus?

Parental care theory assumes that investment in current offspring will trade against future investment. A number of field studies on birds have used clutch size manipulations to demonstrate a survival cost to chick rearing. However, such studies do not account for costs accrued during earlier stages of reproduction because not all aspects of reproductive effort are manipulated by varying the number of nestlings. In this study, we investigate the effect of reproductive effort on female survival in the dung beetle, Onthophagus taurus. By experimentally manipulating mating status and dung availability, we demonstrate that virgin females survive longer than mated females and that the survival of mated females was negatively associated with the number of brood masses produced. Using a novel manipulation of the mating system, we separated the effects of egg production and maternal care on female survival. Previously, we have shown that females provisioning with the assistance of a major male provide relatively less care than unassisted females. However, paternal assistance did not alter the number of brood masses produced and hence the amount of reproductive effort that was allocated to egg production. Therefore, our finding that female survival was increased when receiving paternal assistance provides, to our knowledge, the first definitive evidence that maternal care reduces female lifespan. These results are of major importance to theoretical models on the evolution of parental care.     

Asynchronous hatching provides females with a means for increasing male care but incurs a cost by reducing offspring fitness

In species with biparental care, sexual conflict occurs because the benefit of care depends on the total amount of care provided by the two parents while the cost of care depends on each parent's own contribution. Asynchronous hatching may play a role in mediating the resolution of this conflict over parental care. The sexual conflict hypothesis for the evolution of asynchronous hatching suggests that females adjust hatching patterns in order to increase male parental effort relative to female effort. We tested this hypothesis in the burying beetle Nicrophorus vespilloides by setting up experimental broods with three different hatching patterns: synchronous, asynchronous and highly asynchronous broods. As predicted, we found that males provided care for longer in asynchronous broods whereas the opposite was true of females. However, we did not find any benefit to females of reducing their duration of care in terms of increased lifespan or reduced mass loss during breeding. We found substantial negative effects of hatching asynchrony on offspring fitness as larval mass was lower and fewer larvae survived to dispersal in highly asynchronous broods compared to synchronous or asynchronous broods. Our results suggest that, even though females can increase male parental effort by hatching their broods more asynchronously, females pay a substantial cost from doing so in terms of reducing offspring growth and survival. Thus, females should be under selection to produce a hatching pattern that provides the best possible trade‐off between the benefits of increased male parental effort and the costs due to reduced offspring fitness.     

Staying with the young enhances the fathers’ attractiveness in burying beetles

Studying the relationship between parental and mating effort helps us to understand the evolution of parental care and, consequently, has been the subject of many theoretical and empirical investigations. Using burying beetles as a model, we found no correlation between the intensity of a sexual signal (sex pheromone quantity) and the amount of care provided by males. However, males that were given the opportunity to breed and care for young went on to produce a higher amount of their sexual signal and attracted three times more females in the field than control males that were not given the opportunity to breed. The likely explanation for our finding is that specific aspects of care in burying beetles, that is the defense and preservation of a nutrient rich breeding resource, a small vertebrate cadaver, is not only beneficial for the offspring but also for the adults themselves. Obtaining a good carrion meal possibly enables males to store resources that they can subsequently allocate toward sexual signaling. Collectively, our results highlight that conditions can exist where male participation in brood care has a positive effect on its sexual attractiveness. This in turn might have facilitated the evolution of male assistance in parental care.     

Can low-quality parents exploit their high-quality partners to gain higher fitness?

An individual's optimal investment in parental care potentially depends on many variables, including its future fitness prospects, the expected costs of providing care and its partner's expected or observed parental behaviour. Previous models suggested that low-quality parents could evolve to exploit their high-quality partners by reducing care, leading to the paradoxical prediction that low-quality parents could have higher fitness than their high-quality partners. However, these studies lacked a complete and consistent life-history model. Here, we challenge this result, developing a consistent analytical model of parental care strategies given individual variation in quality, and checking our results using agent-based simulations. In contrast to previous models, we predict that high-quality individuals always outcompete low-quality individuals in fitness terms. However, care effort may differ between high- and low-quality parents in either direction: low-quality individuals care more than high-quality individuals if their baseline mortality is higher, but less if their mortality increases more steeply with increasing care. We also highlight the ambiguity of the term ‘quality’ and stress the need for ‘genealogical consistency’ in evolutionary models.     

Extraterritorial forays and male parental care in hooded warblers

Extrapair paternity is common among many songbird species yet few studies have quantified male extraterritorial foray (ETF) effort and examined potential trade-offs. One potentially important constraint for males is the need to provide parental care. Current models of male extrapair mating tactics propose that males reduce extraterritorial foray effort later in the breeding season because they face a trade-off between feeding nestlings versus pursuing extrapair matings. However, detailed field studies examining the trade-off between paternal care and male extraterritorial forays are lacking. We used radiotelemetry to quantify male extraterritorial foray effort in hooded warblers, Wilsonia citrina, to test the widely held predictions that: (1) males make significantly fewer and shorter forays during the nestling stage relative to other stages (i.e. fertile and incubating stages); and (2) male extraterritorial foray effort is negatively correlated with parental effort. Males made 0.87+/-0.09 forays/h and spent on average 12.2% of their time foraying off territory. Results were equivocal; some data suggested male foray effort decreased in relation to parental care, while other data suggested otherwise. Pairwise tests controlling for (1) extrapair mating opportunity among males and (2) male, territory and social mate quality revealed a possible trade-off between the mean duration and percentage of time in extraterritorial foray versus providing parental care. Conversely, results also revealed (1) no difference in foray rate, foray duration or percentage of time spent off territory over the various stages of the breeding season, (2) no relationship between male foray effort and male feeding rate, and (3) no difference in foray rate in pairwise comparisons, controlling for variability in extrapair mating opportunity and male quality. Overall, the trade-off between providing male parental care and pursuing alternative mating tactics may not be as strong for male hooded warblers as once hypothesized because males dedicated relatively little time to seeking extrapair copulations off territory. Copyright 2000 The Association for the Study of Animal Behaviour.     

Exploration behaviour is not associated with chick provisioning in great tits

In biparental systems, members of the same pair can vary substantially in the amount of parental care they provide to offspring. The extent of this asymmetry should depend on the relative costs and benefits of care. Individual variation in personality is likely to influence this trade-off, and hence is a promising candidate to explain differences in care. In addition, plasticity in parental care may also be associated with personality differences. Using exploration behaviour (EB) as a measure of personality, we investigated these possibilities using both natural and experimental data from a wild population of great tits (Parus major). Contrary to predictions, we found no association between EB and natural variation in provisioning behaviour. Nor was EB linked to responsiveness to experimentally increased brood demand. These results are initially surprising given substantial data from other studies suggesting personality should influence investment in parental care. However, they are consistent with a recent study showing selection on EB is weak and highly context-specific in the focal population. This emphasises the difficulty faced by personality studies attempting to make predictions based on previous work, given that personalities often vary among populations of the same species.     

Parental Responses to Changes in Costs and Benefits Along an Environmental Gradient

We evaluated the effects of dissolved oxygen on offspring survival, parental costs, and the pattern of parental care in Florida flagfish, Jordanella floridae (Cyprinodontidae). Specifically, we quantified (1) embryonic development and survival in the absence of parental care, (2) behavior of non-reproductive adults, and (3) behavior of parental males across a gradient in dissolved oxygen. Embryo developmental rates and survivorship increased with dissolved oxygen, with a relatively sharp increase in survival between medium and high oxygen treatments. Non-reproductive adults increased their frequency of aquatic surface respiration, reduced overall activity, and increased opercular beat rate as oxygen declined, suggesting increased costs of activity with reduced oxygen. Taking these cost measures together, costs appear to increase slowly as oxygen starts to decline and then increase sharply as conditions approach hypoxia. In contrast, parental effort increased gradually with dissolved oxygen. We conclude that the increase in care from low to medium oxygen primarily results from a sharp decline in physiological costs, whereas the continued increase in care from medium to high oxygen primarily results from an increase in offspring value. In addition, our results highlight that the benefits of fanning for offspring are not well understood and that they may increase with oxygen, contrary to what has been previously assumed.