Interaction between parental care and sibling competition: parents enhance offspring growth and exacerbate sibling competition

Species with elaborate parental care often also show intense sibling competition over resources provided by parents, suggesting joint evolution of these two traits. Despite this, the evolution of elaborate parental care and the evolution of intense sibling competition are often studied separately. Here, we examine the interaction between parental food provisioning and sibling competition for resources through the joint manipulation of the presence or absence of parents and brood size in a species with facultative parental care: the burying beetle Nicrophorus vespilloides. The effect of the interaction between the presence or absence of parents and brood size was strong; brood size had a strong effect on growth when parents provided care, but no effect when parents were absent. As in previous studies, offspring grew faster when parents were present than when parents were absent, and offspring grew faster in smaller broods than in larger broods. Our behavioral observations showed that brood size had a negative effect on both the amount of time parents spent providing resources to individual offspring and the offspring's effectiveness of begging, confirming that the level of sibling competition increased with brood size. Furthermore, offspring in larger broods shifted more from begging toward self-feeding as they grew older compared to offspring in small broods. Our study provides novel insights into the joint evolution of parental care and sibling competition, and the evolution of offspring begging signals. We discuss the implications of our results in light of recent theoretical work on the evolution of parental care, sibling competition, and offspring begging signals.     

Parental care masks a density‐dependent shift from cooperation to competition among burying beetle larvae

Studies of siblings have focused mainly on their competitive interactions and to a lesser extent on their cooperation. However, competition and cooperation are at opposite ends on a continuum of possible interactions and the nature of these interactions may be flexible with ecological factors tipping the balance toward competition in some environments and cooperation in others. Here we show that the presence of parental care and the density of larvae on the breeding carcass change the outcome of sibling interactions in burying beetle broods. With full parental care there was a strong negative relationship between larval density and larval mass, consistent with sibling competition for resources. In the absence of care, initial increases in larval density had beneficial effects on larval mass but further increases in larval density reduced larval mass. This likely reflects a density‐dependent shift between cooperation and competition. In a second experiment, we manipulated larval density and removed parental care. We found that the ability of larvae to penetrate the breeding carcass increased with larval density and that feeding within the carcass resulted in heavier larvae than feeding outside the carcass. However, larval density did not influence carcass decay.     

Inbreeding depression in an insect with maternal care: influences of family interactions,life stage and offspring sex

Although inbreeding is commonly known to depress individual fitness, the severity of inbreeding depression varies considerably across species. Among the factors contributing to this variation, family interactions, life stage and sex of offspring have been proposed, but their joint influence on inbreeding depression remains poorly understood. Here, we demonstrate that these three factors jointly shape inbreeding depression in the European earwig, Forficula auricularia. Using a series of cross‐breeding, split‐clutch and brood size manipulation experiments conducted over two generations, we first showed that sib mating (leading to inbred offspring) did not influence the reproductive success of earwig parents. Second, the presence of tending mothers and the strength of sibling competition (i.e. brood size) did not influence the expression of inbreeding depression in the inbred offspring. By contrast, our results revealed that inbreeding dramatically depressed the reproductive success of inbred adult male offspring, but only had little effect on the reproductive success of inbred adult female offspring. Overall, this study demonstrates limited effects of family interactions on inbreeding depression in this species and emphasizes the importance of disentangling effects of sib mating early and late during development to better understand the evolution of mating systems and population dynamics.     

Fetal microchimerism and maternal health: A review and evolutionary analysis of cooperation and conflict beyond the womb

The presence of fetal cells has been associated with both positive and negative effects on maternal health. These paradoxical effects may be due to the fact that maternal and offspring fitness interests are aligned in certain domains and conflicting in others, which may have led to the evolution of fetal microchimeric phenotypes that can manipulate maternal tissues. We use cooperation and conflict theory to generate testable predictions about domains in which fetal microchimerism may enhance maternal health and those in which it may be detrimental. This framework suggests that fetal cells may function both to contribute to maternal somatic maintenance (e.g. wound healing) and to manipulate maternal physiology to enhance resource transmission to offspring (e.g. enhancing milk production). In this review, we use an evolutionary framework to make testable predictions about the role of fetal microchimerism in lactation, thyroid function, autoimmune disease, cancer and maternal emotional, and psychological health. Also watch the Video Abstract .     

Costs and benefits of polyandry in a placental poeciliid fish Heterandria formosa are in accordance with the parent-offspring conflict theory of placentation

In viviparous species, a conflict over maternal resource allocation may arise between mothers and embryos, between siblings, and between maternal and paternal genes within an embryo due to relatedness asymmetries. We performed two experiments to study the effects of polyandry and brood relatedness on offspring growth in a placental fish (Heterandria formosa). Polyandry was beneficial as it increased the probability of pregnancy, possibly to avoid genetic incompatibility. However, females mated to four males produced offspring that had a longer maturation time than those of monandrous females. When within-brood relatedness was manipulated, the size of the newborn offspring decreased with time in low-relatedness treatment, whereas in highly related broods, offspring size was constant. Low within-brood relatedness may lead to less cooperative offspring in terms of resource extraction from the mother, which may lead to impaired development during gestation. Offspring conflict may thus reduce the benefits of polyandry in viviparous species.     

The other facets of family life and their role in the evolution of animal sociality

Family life forms an integral part of the life history of species across the animal kingdom and plays a crucial role in the evolution of animal sociality. Our current understanding of family life, however, is almost exclusively based on studies that (i) focus on parental care and associated family interactions (such as those arising from sibling rivalry and parent‐offspring conflict), and (ii) investigate these phenomena in the advanced family systems of mammals, birds, and eusocial insects. Here, we argue that these historical biases have fostered the neglect of key processes shaping social life in ancestral family systems, and thus profoundly hamper our understanding of the (early) evolution of family life. Based on a comprehensive survey of the literature, we first illustrate that the strong focus on parental care in advanced social systems has deflected scrutiny of other important social processes such as sibling cooperation, parent–offspring competition and offspring assistance. We then show that accounting for these neglected processes – and their changing role over time – could profoundly alter our understanding of the origin and subsequent evolution of family life. Finally, we outline how this ‘diachronic’ perspective on the evolution of family living provides novel insights into general processes driving the evolution of animal sociality. Overall, we infer that the explicit consideration of thus‐far neglected facets of family life, together with their study across the whole diversity of family systems, are crucial to advance our understanding of the processes that shape the evolution of social life.     

Family dynamics through time: brood reduction followed by parental compensation with aggression and favouritism

Parental food allocation in birds has long been a focal point for life history and parent–offspring conflict theories. In asynchronously hatching species, parents are thought to either adjust brood size through death of marginal offspring (brood reduction), or feed the disadvantaged chicks to reduce the competitive hierarchy (parental compensation). Here, we show that parent American coots (Fulica americana) practice both strategies by switching from brood reduction to compensation across time. Late‐hatching chicks suffer higher mortality only for the first few days after hatching. Later, parents begin to exhibit parental aggression towards older chicks and each parent favours a single chick, both of which are typically the youngest of the surviving offspring. The late‐hatched survivors can equal or exceed their older siblings in size prior to independence. A mixed allocation strategy allows parents to compensate for the costs of competitive hierarchies while gaining the benefits of hatching asynchrony.     

Balancing competing life‐stage requirements in salmon habitat rehabilitation: between a rock and a hard place

Gravel augmentation is often applied to rivers and streams to rehabilitate salmonid spawning and incubation habitat. However, the effect of gravel size on salmon spawning utilization and embryo survival during incubation is not well understood. We conducted an experiment on a regulated and previously mined Northern California salmonid‐bearing stream in which different sized gravel (small, medium, and large) patches were placed into the stream's degraded spawning reach. We documented Oncorhynchus tshawytscha (Chinook salmon) spawning activity within the three gravel sizes for two seasons. In addition, we deployed Chinook salmon embryos into each gravel size patch and allowed them to incubate until estimated emergence time. Although all experimental gravel sizes were predicted to be within the spawning population's mobilization capabilities, model results indicated the probability of salmon building redds decreased as substrate size increased. Conversely, embryo survival increased as gravel size increased. A possible mechanism of disparate Chinook salmon embryo survival is provided by an observed decrease in embryo survival correlating with greater presence of embryo predators (leeches), which are associated with smaller gravel. Our results indicate a parent‐offspring conflict in optimal spawning gravel size for Chinook salmon, and suggest that an intermediate gravel size would maximize overall reproductive success across both spawning and incubation life stages.     

The positive correlation between maternal size and offspring size: fitting pieces of a life‐history puzzle

The evolution of investment per offspring (I) is often viewed through the lens of the classic theory, in which variation among individuals in a population is not expected. A substantial departure from this prediction arises in the form of correlations between maternal body size and I, which are observed within populations in virtually all taxonomic groups. Based on the generality of this observation, we suggest it is caused by a common underlying mechanism. We pursue a unifying explanation for this pattern by reviewing all theoretical models that attempt to explain it. We assess the generality of the mechanism upon which each model is based, and the extent to which data support its predictions. Two classes of adaptive models are identified: models that assume that the correlation arises from maternal influences on the relationship between I and offspring fitness [w(I)], and those that assume that maternal size influences the relationship between I and maternal fitness [W(I)]. The weight of evidence suggests that maternal influences on w(I) are probably not very general, and even for taxa where maternal influences on w(I) are likely, experiments fail to support model predictions. Models that assume that W(I) varies with maternal size appear to offer more generality, but the current challenge is to identify a specific and general mechanism upon which W(I) varies predictably with maternal size. Recent theory suggests the exciting possibility that a yet unknown mechanism modifies the offspring size–number trade‐off function in a manner that is predictable with respect to maternal size, such that W(I) varies with size. We identify two promising avenues of inquiry. First, the trade‐off might be modified by energetic costs that are associated with the initiation of reproduction (‘overhead costs’) and that scale with I, and future work could investigate what specific overhead costs are generally associated with reproduction and whether these costs scale with I. Second, the trade‐off might be modified by virtue of condition‐dependent offspring provisioning coupled with metabolic factors, and future work could investigate the proximate cause of, and generality of, condition‐dependent offspring provisioning. Finally, drawing on the existing literature, we suggest that maternal size per se is not causatively related to variation in I, and the mechanism involved in the correlation is instead linked to maternal nutritional status or maternal condition, which is usually correlated with maternal size. Using manipulative experiments to elucidate why females with high nutritional status typically produce large offspring might help explain what specific mechanism underlies the maternal‐size correlation.     

Two alternatives to the stress‐gradient hypothesis at the edge of life: the collapse of facilitation and the switch from facilitation to competition

New evidence demonstrates that facilitation plays a crucial role even at the edge of life in Maritime Antarctica. These findings are interpreted as support for the stress‐gradient hypothesis (SGH) – a dominant theory in plant community ecology that predicts that the frequency of facilitation directly increases with stress. A recent development to this theory, however, proposed that facilitation often collapses at the extreme end of stress and physical disturbance gradients. In this paper, we clarify the current debate on the importance of plant interactions at the edge of life by illustrating the necessity of separating the two alternatives to the SGH, namely the collapse of facilitation, and the switch from facilitation to competition occurring in water‐stressed ecosystems. These two different alternatives to the SGH are currently often amalgamated with each other, which has led to confusion in recent literature. We propose that the collapse of facilitation is generally due to a decrease in the effect of the nurse plant species, whilst the switch from facilitation to competition is driven by environmental conditions and strategy of the response species. A clear separation between those two alternatives is particularly crucial for predicting the role of plant–plant interactions in mediating species responses to global change.     

Future warmer seas: increased stress and susceptibility to grazing in seedlings of a marine habitat‐forming species

Increases in seawater temperature are expected to have negative consequences for marine organisms. Beyond individual effects, species‐specific differences in thermal tolerance are predicted to modify species interactions and increase the strength of top‐down effects, particularly in plant–herbivore interactions. Shifts in trophic interactions will be especially important when affecting habitat‐forming species such as seagrasses, as the consequences on their abundance will cascade throughout the food web. Seagrasses are a major component of coastal ecosystems offering important ecosystem services, but are threatened by multiple anthropogenic stressors, including warming. The mechanistic understanding of seagrass responses to warming at multiple scales of organization remains largely unexplored, especially in early‐life stages such as seedlings. Yet, these early‐life stages are critical for seagrass expansion processes and adaptation to climate change. In this study, we determined the effects of a 3 month experimental exposure to present and predicted mean summer SST of the Mediterranean Sea (25°C, 27°C, and 29°C) on the photophysiology, size, and ecology (i.e., plant‐herbivore interactions) of seedlings of the seagrass Posidonia oceanica. Warming resulted in increased mortality, leaf necrosis, and respiration as well as lower carbohydrate reserves in the seed, the main storage organ in seedlings. Aboveground biomass and root growth were also limited with warming, which could hamper seedling establishment success. Furthermore, warming increased the susceptibility to consumption by grazers, likely due to lower leaf fiber content and thickness. Our results indicate that warming will negatively affect seagrass seedlings through multiple direct and indirect pathways: increased stress, reduced establishment potential, lower storage of carbohydrate reserves, and increased susceptibly to consumption. This work provides a significant step forward in understanding the major mechanisms that will drive the capacity of seagrass seedlings to adapt and survive to warming, highlighting the potential additive effects that herbivory will have on ultimately determining seedling success.     

Mutations in amyloid precursor protein and presenilin-1 genes increase the basal oxidative stress in murine neuronal cells and lead to increased sensitivity to oxidative stress mediated by amyloid beta-peptide (1-42), HO and kainic acid: implications for Alzheimer's disease

Oxidative stress is observed in Alzheimer's disease (AD) brain, including protein oxidation and lipid peroxidation. One of the major pathological hallmarks of AD is the brain deposition of amyloid beta-peptide (Abeta). This 42-mer peptide is derived from the beta-amyloid precursor protein (APP) and is associated with oxidative stress in vitro and in vivo. Mutations in the PS-1 and APP genes, which increase production of the highly amyloidogenic amyloid beta-peptide (Abeta42), are the major causes of early onset familial AD. Several lines of evidence suggest that enhanced oxidative stress, inflammation, and apoptosis play important roles in the pathogenesis of AD. In the present study, primary neuronal cultures from knock-in mice expressing mutant human PS-1 and APP were compared with those from wild-type mice, in the presence or absence of various oxidizing agents, viz, Abeta(1-42), H2O2 and kainic acid (KA). APP/PS-1 double mutant neurons displayed a significant basal increase in oxidative stress as measured by protein oxidation, lipid peroxidation, and 3-nitrotyrosine when compared with the wild-type neurons (p < 0.0005). Elevated levels of human APP, PS-1 and Abeta(1-42) were found in APP/PS-1 cultures compared with wild-type neurons. APP/PS-1 double mutant neuron cultures exhibited increased vulnerability to oxidative stress, mitochondrial dysfunction and apoptosis induced by Abeta(1-42), H2O2 and KA compared with wild-type neuronal cultures. The results are consonant with the hypothesis that Abeta(1-42)-associated oxidative stress and increased vulnerability to oxidative stress may contribute significantly to neuronal apoptosis and death in familial early onset AD.