Compensating for delayed hatching across consecutive life‐history stages in an amphibian

Environmental conditions experienced early in the ontogeny can have a strong impact on individual fitness and performance later in life. Organisms may counteract the negative effects of poor developmental conditions by developing compensatory responses in growth and development. However, previous studies on compensatory responses have largely ignored the effects that poor embryonic conditions could have during the later life stages. In this study, we examined the effects of artificially delayed development in early life over two later life history transitions by investigating the compensatory growth of larval moor frogs Rana arvalis in response to temperature variation during embryonic development, and the associated costs during the larval ′and postmetamorphic stages. Low temperature during embryonic stage lead to delayed hatching at smaller size. The groups with delayed embryonic development showed strong compensatory growth during the larval stage, and reached similar metamorphic size than the controls in a shorter time. However, the most strongly delayed group was not able to fully catch up the total development time. These compensatory responses were found in the absence of photoperiod cues indicating that the delay in embryonic development was sufficient to initiate the compensatory response in larval growth and development. No apparent costs of compensatory growth were detected in terms of morphology or locomotor performance at the juvenile stage. We found that compensatory responses can be activated as early as at the embryonic stage and extend over several consecutive life history transitions, mitigating the effects of poor conditions experienced early in development. Potential short‐term costs in natural environments and the occurrence of long‐term costs, which prevent the generalisation of a faster larval life style, are discussed.     

Linking life‐history theory and metabolic theory explains the offspring size‐temperature relationship

Temperature often affects maternal investment in offspring. Across and within species, mothers in colder environments generally produce larger offspring than mothers in warmer environments, but the underlying drivers of this relationship remain unresolved. We formally evaluated the ubiquity of the temperature–offspring size relationship and found strong support for a negative relationship across a wide variety of ectotherms. We then tested an explanation for this relationship that formally links life‐history and metabolic theories. We estimated the costs of development across temperatures using a series of laboratory experiments on model organisms, and a meta‐analysis across 72 species of ectotherms spanning five phyla. We found that both metabolic and developmental rates increase with temperature, but developmental rate is more temperature sensitive than metabolic rate, such that the overall costs of development decrease with temperature. Hence, within a species’ natural temperature range, development at relatively cooler temperatures requires mothers to produce larger, better provisioned offspring.     

Eco‐evolutionary dynamics in response to selection on life‐history

Understanding the consequences of environmental change on ecological and evolutionary dynamics is inherently problematic because of the complex interplay between them. Using invertebrates in microcosms, we characterise phenotypic, population and evolutionary dynamics before, during and after exposure to a novel environment and harvesting over 20 generations. We demonstrate an evolved change in life‐history traits (the age‐ and size‐at‐maturity, and survival to maturity) in response to selection caused by environmental change (wild to laboratory) and to harvesting (juvenile or adult). Life‐history evolution, which drives changes in population growth rate and thus population dynamics, includes an increase in age‐to‐maturity of 76% (from 12.5 to 22 days) in the unharvested populations as they adapt to the new environment. Evolutionary responses to harvesting are outweighed by the response to environmental change (~ 1.4 vs. 4% change in age‐at‐maturity per generation). The adaptive response to environmental change converts a negative population growth trajectory into a positive one: an example of evolutionary rescue.     

PEGylation of bacteriophages increases blood circulation time and reduces T‐helper type 1 immune response

The increasing occurrence of antibiotic‐resistant pathogens is of growing concern, and must be counteracted by alternative antimicrobial treatments. Bacteriophages represent the natural enemies of bacteria. However, the strong immune response following application of phages and rapid clearance from the blood stream are hurdles which need to be overcome. Towards our goal to render phages less immunogenic and prolong blood circulation time, we have chemically modified intact bacteriophages by conjugation of the non‐immunogenic polymer monomethoxy‐polyethylene glycol (mPEG) to virus proteins. As a proof of concept, we have used two different polyvalent and strictly virulent phages of the Myoviridae, representing typical candidates for therapeutical approaches: Felix‐O1 (infects Salmonella) and A511 (infects Listeria). Loss of phage infectivity after PEGylation was found to be proportional to the degree of modification, and could be conveniently controlled by adjusting the PEG concentration. When injected into naïve mice, PEGylated phages showed a strong increase in circulation half‐life, whereas challenge of immunized mice did not reveal a significant difference. Our results suggest that the prolonged half‐life is due to decreased susceptibility to innate immunity as well as avoidance of cellular defence mechanisms. PEGylated viruses elicited significantly reduced levels of T‐helper type 1‐associated cytokine release (IFN‐γ and IL‐6), in both naïve and immunized mice. This is the first study demonstrating that PEGylation can increases survival of infective phage by delaying immune responses, and indicates that this approach can increase efficacy of bacteriophage therapy.     

Parasitism and constitutive defence costs to host life‐history traits in a parasitoid–host interaction

1. The level of an organism's investment in defences against natural enemies depends on the fitness costs of resisting parasitism and on the costs of maintaining defences in the absence of infection. Heritable variation in resistance suggests that costs exist, but very little is known about the nature or magnitude of these costs in natural populations of animals. 2. A powerful technique for identifying trade‐offs between fitness components is the study of correlated responses to artificial selection. We selected for increased resistance in the Indian meal moth, Plodia interpunctella, following parasitism by the koinobiont parasitoid, Venturia canescens, and measured the cost of resistance to parasitism and the cost of maintaining resistance in the absence of immune challenge during the next generation. 3. Parasitism decreased larval host size, growth, and developmental time and was significantly negatively correlated with the size of surviving host adults. Larvae of the next generation also had a reduced developmental period, whilst the duration of the invulnerable pupal instar was increased. There was no effect on host adult size and related fecundity in the F₁ generation.     

Cognitive costs of reproduction: life‐history trade‐offs explain cognitive decline during pregnancy in women

Life‐history theory predicts that access to limited resources leads to trade‐offs between competing body functions. Women, who face higher costs of reproduction when compared to men, should be especially vulnerable to these trade‐offs. We propose the ‘cognitive costs of reproduction hypothesis’, which states that energy trade‐offs imposed by reproduction may lead to a decline in maternal cognitive function during gestation. In particular, we hypothesize that the decline in cognitive function frequently observed during pregnancy is associated with the allocation of resources between the competing energetic requirements of the mother's brain and the developing foetus. Several distinctive anatomical and physiological features including a high metabolic rate of the brain, large infant size, specific anatomical features of the placenta and trophoblast, and the lack of maternal control over glucose flow through the placenta make the occurrence of these trade‐offs likely. Herein, we review several lines of evidence for trade‐offs between gestation and cognition that are related to: (i) energy metabolism during reproduction; (ii) energy metabolism of the human brain; (iii) links between energy metabolism and cognitive function; and (iv) links between gestation and cognitive function. We also review evidence for the important roles of cortisol, corticotropin‐releasing hormone and sex hormones in mediating the effects of gestation on cognition, and we discuss possible neurophysiological mechanisms underlying the observed effects. The evidence supports the view that energy trade‐offs between foetal growth and maternal endocrine and brain function lead to changes in maternal cognition, and that this phenomenon is mediated by neuroendocrine mechanisms involving the hypothalamic–pituitary–adrenal axis, brainstem nucleus locus coeruleus and hippocampus.     

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.     

Social systems and life‐history characteristics of mongooses

The diversity of extant carnivores provides valuable opportunities for comparative research to illuminate general patterns of mammalian social evolution. Recent field studies on mongooses (Herpestidae), in particular, have generated detailed behavioural and demographic data allowing tests of assumptions and predictions of theories of social evolution. The first studies of the social systems of their closest relatives, the Malagasy Eupleridae, also have been initiated. The literature on mongooses was last reviewed over 25 years ago. In this review, we summarise the current state of knowledge on the social organisation, mating systems and social structure (especially competition and cooperation) of the two mongoose families. Our second aim is to evaluate the contributions of these studies to a better understanding of mammalian social evolution in general. Based on published reports or anecdotal information, we can classify 16 of the 34 species of Herpestidae as solitary and nine as group‐living; there are insufficient data available for the remainder. There is a strong phylogenetic signal of sociality with permanent complex groups being limited to the genera Crossarchus, Helogale, Liberiictis, Mungos, and Suricata. Our review also indicates that studies of solitary and social mongooses have been conducted within different theoretical frameworks: whereas solitary species and transitions to gregariousness have been mainly investigated in relation to ecological determinants, the study of social patterns of highly social mongooses has instead been based on reproductive skew theory. In some group‐living species, group size and composition were found to determine reproductive competition and cooperative breeding through group augmentation. Infanticide risk and inbreeding avoidance connect social organisation and social structure with reproductive tactics and life histories, but their specific impact on mongoose sociality is still difficult to evaluate. However, the level of reproductive skew in social mongooses is not only determined by the costs and benefits of suppressing each other's breeding attempts, but also influenced by resource abundance. Thus, dispersal, as a consequence of eviction, is also linked to the costs of co‐breeding in the context of food competition. By linking these facts, we show that the socio‐ecological model and reproductive skew theory share some determinants of social patterns. We also conclude that due to their long bio‐geographical isolation and divergent selection pressures, future studies of the social systems of the Eupleridae will be of great value for the elucidation of general patterns in carnivore social evolution.     

Immune deployment increases larval vulnerability to predators and inhibits adult life‐history traits in a dragonfly

While deploying immune defences early in ontogeny can trade‐off with the production and maintenance of other important traits across the entire life cycle, it remains largely unexplored how features of the environment shape the magnitude or presence of these lifetime costs. Greater predation risk during the juvenile stage may particularly influence such costs by (1) magnifying the survival costs that arise from any handicap of juvenile avoidance traits and/or (2) intensifying allocation trade‐offs with important adult traits. Here, we tested for predator‐dependent costs of immune deployment within and across life stages using the dragonfly, Pachydiplax longipennis. We first examined how larval immune deployment affected two traits associated with larval vulnerability to predators: escape distance and foraging under predation risk. Larvae that were induced to mount an immune response had shorter escape distances but lower foraging activity in the presence of predator cues. We also induced immune responses in larvae and reared them through emergence in mesocosms that differed in the presence of large predatory dragonfly larvae (Aeshnidae spp.). Immune‐challenged larvae had later emergence overall and lower survival in pools with predators. Immune‐challenged males were also smaller at emergence and developed less sexually selected melanin wing coloration, but these effects were independent of predator treatment. Overall, these results highlight how mounting an immune defence early in ontogeny can have substantial ecological and physiological costs that manifest both within and across life stages.     

The demographic and life‐history costs of fear: Trait‐mediated effects of threat of predation on Aedes triseriatus

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Among‐individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life‐history traits in the garter snake Thamnophis elegans

Accumulating evidence suggests that within‐individual plasticity of behavioural and physiological traits is limited, resulting in stable among‐individual differences in these aspects of the phenotype. Furthermore, these traits often covary within individuals, resulting in a continuum of correlated phenotypic variation among individuals within populations and species. This heterogeneity, in turn, affects individual fitness and can have cross‐generational effects. Patterns of trait covariation, among‐individual differences, and subsequent fitness consequences have long been recognized in reptiles. Here, we provide a test of patterns of among‐individual heterogeneity in behaviour and physiology and subsequent effects on reproduction and offspring fitness in the garter snake Thamnophis elegans. We find that measures of activity levels vary among individuals and are consistent within individuals in reproductive female snakes, indicating stable behavioural phenotypes. Blood hormone and glucose concentrations are not as stable within individuals, indicating that these traits do not describe consistent physiological phenotypes. Nonetheless, the major axes of variation in maternal traits describe behavioural and physiological phenotypes that interact to predict offspring body condition and mass at birth. This differential allocation of energy to offspring, in turn, strongly influences subsequent offspring growth and survival. This pattern suggests the potential for strong selection on phenotypes defined by behaviour–physiology interactions.     

The early‐life environment and individual plasticity in life‐history traits

We tested whether the early‐life environment can influence the extent of individual plasticity in a life‐history trait. We asked: can the early‐life environment explain why, in response to the same adult environmental cue, some individuals invest more than others in current reproduction? Moreover, can it additionally explain why investment in current reproduction trades off against survival in some individuals, but is positively correlated with survival in others? We addressed these questions using the burying beetle, which breeds on small carcasses and sometimes carries phoretic mites. These mites breed alongside the beetle, on the same resource, and are a key component of the beetle's early‐life environment. We exposed female beetles to mites twice during their lives: during their development as larvae and again as adults during their first reproductive event. We measured investment in current reproduction by quantifying average larval mass and recorded the female's life span after breeding to quantify survival. We found no effect of either developing or breeding alongside mites on female reproductive investment, nor on her life span, nor did developing alongside mites influence her size. In post hoc analyses, where we considered the effect of mite number (rather than their mere presence/absence) during the female's adult breeding event, we found that females invested more in current reproduction when exposed to greater mite densities during reproduction, but only if they had been exposed to mites during development as well. Otherwise, they invested less in larvae at greater mite densities. Furthermore, females that had developed with mites exhibited a trade‐off between investment in current reproduction and future survival, whereas these traits were positively correlated in females that had developed without mites. The early‐life environment thus generates individual variation in life‐history plasticity. We discuss whether this is because mites influence the resources available to developing young or serve as important environmental cues.     

Macroevolutionary evidence suggests trait‐dependent coevolution between behavior and life‐history

Species with fast life‐histories typically prioritize current over future reproductive events, compared to species with slow life‐histories. These species therefore require greater energetic input into reproduction, and also likely have less time to realize their reproductive potential. Hence, behaviors that increase access to both resources and mating opportunities, at a cost of increased mortality risk, could coevolve with the pace of life‐history. However, whether this prediction holds across species, remains untested under standardized conditions. Here, we test how risky behaviors, which facilitate access to resources and mating opportunities (i.e., activity, boldness, and aggression), along with metabolic rate, coevolve with the pace of life‐history across 20 species of killifish that present remarkable divergences in the pace of life‐history. We found a positive association between the pace of life‐history and aggression, but interestingly not with other behavioral traits or metabolic rate. Aggression is linked to interference competition, and in killifishes is often employed to secure mates, while activity and boldness are more relevant for exploiting energetic resources. Our results suggest that the trade‐off between current and future reproduction plays a more prominent role in shaping mating behavior, while behaviors related to energy acquisition may be influenced by ecological factors.     

Landscape‐scale life‐history gradients in New Zealand freshwater fish

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Close‐kin mating,but not inbred parents,reduces hatching rates and offspring quality in a threatened tortoise

Inbreeding depression, the reduction in fitness due to mating of related individuals, is of particular conservation concern in species with small, isolated populations. Although inbreeding depression is widespread in natural populations, long‐lived species may be buffered from its effects during population declines due to long generation times and thus are less likely to have evolved mechanisms of inbreeding avoidance than species with shorter generation times. However, empirical evidence of the consequences of inbreeding in threatened, long‐lived species is limited. In this study, we leverage a well‐studied population of gopher tortoises, Gopherus polyphemus, to examine the role of inbreeding depression and the potential for behavioural inbreeding avoidance in a natural population of a long‐lived species. We tested the hypothesis that increased parental inbreeding leads to reduced hatching rates and offspring quality. Additionally, we tested for evidence of inbreeding avoidance. We found that high parental relatedness results in offspring with lower quality and that high parental relatedness is correlated with reduced hatching success. However, we found that hatching success and offspring quality increase with maternal inbreeding, likely due to highly inbred females mating with more distantly related males. We did not find evidence for inbreeding avoidance in males and outbred females, suggesting sex‐specific evolutionary trade‐offs may have driven the evolution of mating behaviour. Our results demonstrate inbreeding depression in a long‐lived species and that the evolution of inbreeding avoidance is shaped by multiple selective forces.     

Predators modify the temperature dependence of life‐history trade‐offs

Although life histories are shaped by temperature and predation, their joint influence on the interdependence of life‐history traits is poorly understood. Shifts in one life‐history trait often necessitate shifts in another—structured in some cases by trade‐offs—leading to differing life‐history strategies among environments. The offspring size–number trade‐off connects three traits whereby a constant reproductive allocation (R) constrains how the number (O) and size (S) of offspring change. Increasing temperature and size‐independent predation decrease size at and time to reproduction which can lower R through reduced time for resource accrual or size‐constrained fecundity. We investigated how O, S, and R in a clonal population of Daphnia magna change across their first three clutches with temperature and size‐independent predation risk. Early in ontogeny, increased temperature moved O and S along a trade‐off curve (constant R) toward fewer larger offspring. Later in ontogeny, increased temperature reduced R in the no‐predator treatment through disproportionate decreases in O relative to S. In the predation treatment, R likewise decreased at warmer temperatures but to a lesser degree and more readily traded off S for O whereby the third clutch showed a constant allocation strategy of O versus S with decreasing R. Ontogenetic shifts in S and O rotated in a counterclockwise fashion as temperature increased and more drastically under risk of predation. These results show that predation risk can alter the temperature dependence of traits and their interactions through trade‐offs.     

Trade‐offs between life‐history traits at range‐edge and central locations

The allocation of resources to different life‐history traits should represent the best compromise in fitness investment for organisms in their local environment. When resources are limiting, the investment in a specific trait must carry a cost that is expressed in trade‐offs with other traits. In this study, the relative investment in the fitness‐related traits, growth, reproduction and defence were compared at central and range‐edge locations, using the seaweed Ascophyllum nodosum as a model system. Individual growth rates were similar at both sites, whereas edge populations showed a higher relative investment in reproduction (demonstrated by a higher reproductive allocation and extended reproductive periods) when compared to central populations that invested more in defence. These results show the capability of A. nodosum to differentially allocate resources for different traits under different habitat conditions, suggesting that reproduction and defence have different fitness values under the specific living conditions experienced at edge and central locations. However, ongoing climate change may threaten edge populations by increasing the selective pressure on specific traits, forcing these populations to lower the investment in other traits that are also potentially important for population fitness.