Phenotypic plasticity in adult life-history strategies compensates for a poor start in life in Trinidadian guppies (Poecilia reticulata)

Low food availability during early growth and development can have long-term negative consequences for reproductive success. Phenotypic plasticity in adult life-history decisions may help to mitigate these potential costs, yet adult life-history responses to juvenile food conditions remain largely unexplored. I used a food-manipulation experiment with female Trinidadian guppies (Poecilia reticulata) to examine age-related changes in adult life-history responses to early food conditions, whether these responses varied across different adult food conditions, and how these responses affected overall reproductive success. Guppy females reared on low food as juveniles matured at a later age, at a smaller size, and with less energy reserves than females reared on high food as juveniles. In response to this setback, they changed their investment in growth, reproduction, and fat storage throughout the adult stage such that they were able to catch up in body size, increase their reproductive output, and restore their energy reserves to levels comparable to those of females reared on high food as juveniles. The net effect was that adult female guppies did not merely mitigate but surprisingly were able to fully compensate for the potential long-term negative effects of poor juvenile food conditions on reproductive success.     

The role of predation in variation in body shape in guppies Poecilia reticulata: a comparison of field and common garden phenotypes

The body shapes of both wild-caught and laboratory-reared male and female Trinidadian guppies Poecilia reticulata from two low-predation and two high-predation populations were studied, but predation regime did not seem to be the most important factor affecting body shape. Instead, complicated patterns of plasticity in body shape among populations and the sexes were found. In particular, populations differed in the depth of the caudal peduncle, which is the muscular region just anterior to the tail fin rays and from which most swimming power is generated. Strikingly, the direction of population differences in caudal peduncle depth observed in wild-caught individuals was reversed when P. reticulata were raised in a common laboratory environment.     

Maternal developmental stress reduces reproductive success of female offspring in zebra finches

Environmental factors play a key role in the expression of phenotypic traits and life-history decisions, specifically when they act during early development. In birds, brood size is a main environmental factor affecting development. Experimental manipulation of brood sizes can result in reduced offspring condition, indicating that developmental deficits in enlarged broods have consequences within the affected generation. Yet, it is unclear whether stress during early development can have fitness consequences projecting into the next generation. To study such trans-generational fitness effects, we bred female zebra finches, Taeniopygia guttata, whose mothers had been raised in different experimental brood sizes. We found that adult females were increasingly smaller with increasing experimental brood size in which their mother had been raised. Furthermore, reproductive success at hatching and fledging covaried negatively with the experimental brood size in which their mothers were raised. These results illustrate that early developmental stress can have long-lasting effects affecting reproductive success of future generations. Such trans-generational effects can be life-history responses adapted to environmental conditions experienced early in life.     

Male mating behaviour and sperm production characteristics under varying sperm competition risk in guppies

Since natural populations of guppies, Poecilia reticulata, often differ from one another in social structure, the intensity of sperm competition is likely to vary between localities. Guppies are promiscuous, with female choice for colourful males playing a central role in the mating system. In addition, male guppies use forced copulations to circumvent female choice. Both methods of copulation are used interchangeably by individual males, but the degree to which either is used may depend on the social environment into which males are born. Here we show that male mating behaviour varies according to the rearing sex ratio: when reared in male-biased groups, males performed more forced copulations and fewer courtship displays but showed the opposite pattern of behaviour when reared in female-biased groups. Our prediction, based on sperm competition theory, that stripped sperm number would reflect social structure was not supported by our results. Instead, the overall level of sexual activity (gonopodial thrusts+sigmoid displays) was a better predictor of sperm number in the different groups of males. Rearing density, where sex ratio was controlled, did not significantly affect male mating behaviour or sperm traits. Males reared under the different sex ratios continued to show their characteristic behaviour patterns when placed in equal sex ratio tanks. We conclude, therefore, that males adopt mating strategies to suit their social environment, and that these strategies remain fixed, for short periods at least, if population structure changes. Copyright 1999 The Association for the Study of Animal Behaviour.     

Environmental factors influencing adult sex ratio in Poecilia reticulata: laboratory experiments

The potential causes of adult sex ratio variation in guppies Poecilia reticulata were tested in laboratory experiments that evaluated the mortality rates of male and female P. reticulata exposed to potential predators (Hart's rivulus Rivulus hartii and freshwater prawns Macrobrachium crenulatum) and to different resource levels. Poecilia reticulata mortality increased in the presence of R. hartii and M. crenulatum, and low resource levels had an effect on mortality only in the presence of M. crenulatum. Rivulus hartii preyed more often on male than on female P. reticulata, and this sex-biased predation was not simply the result of males being smaller than females. In contrast, no sex-biased mortality was attributable to M. crenulatum or low resource levels.     

Psychopathy and developmental instability

Psychopaths are manipulative, impulsive, and callous individuals with long histories of antisocial behavior. Two models have guided the study of psychopathy. One suggests that psychopathy is a psychopathology, i.e., the outcome of defective or perturbed development. A second suggests that psychopathy is a life-history strategy of social defection and aggression that was reproductively viable in the environment of evolutionary adaptedness (EEA). These two models make different predictions with regard to the presence of signs of perturbations or instability in the development of psychopaths. In Study 1, we obtained data on prenatal, perinatal, and neonatal signs of developmental perturbations from the clinical files of 643 nonpsychopathic and 157 psychopathic male offenders. In Study 2, we measured fluctuating asymmetry (FA, a concurrent sign of past developmental perturbations) in 15 psychopathic male offenders, 25 nonpsychopathic male offenders, and 31 male nonoffenders. Psychopathic offenders scored lower than nonpsychopathic offenders on obstetrical problems and FA; both psychopathic and nonpsychopathic offenders scored higher than nonoffenders on FA. The five offenders from Study 2 meeting the most stringent criteria for psychopathy were similar to nonoffenders with regard to FA and had the lowest asymmetry scores among offenders. These results provide no support for psychopathological models of psychopathy and partial support for life-history strategy models.     

Male sexual harassment alters female social behaviour towards other females

Male harassment of females to gain mating opportunities is a consequence of an evolutionary conflict of interest between the sexes over reproduction and is common among sexually reproducing species. Male Trinidadian guppies Poecilia reticulata spend a large proportion of their time harassing females for copulations and their presence in female social groups has been shown to disrupt female-female social networks and the propensity for females to develop social recognition based on familiarity. In this study, we investigate the behavioural mechanisms that may lead to this disruption of female sociality. Using two experiments, we test the hypothesis that male presence will directly affect social behaviours expressed by females towards other females in the population. In experiment one, we tested for an effect of male presence on female shoaling behaviour and found that, in the presence of a free-swimming male guppy, females spent shorter amounts of time with other females than when in the presence of a free-swimming female guppy. In experiment two, we tested for an effect of male presence on the incidence of aggressive behaviour among female guppies. When males were present in a shoal, females exhibited increased levels of overall aggression towards other females compared with female only shoals. Our work provides direct evidence that the presence of sexually harassing males alters female-female social behaviour, an effect that we expect will be recurrent across taxonomic groups.     

Separate and combined effects of nutrition during juvenile and sexual development on female life-history trajectories: the thrifty phenotype in a cockroach

We have yet to understand fully how conditions during different periods of development interact to influence life-history structure. Can the negative effects of poor juvenile nutrition be overcome by a good adult diet, or are life-history strategies set by early experience? Here, we tested the influence and interaction of different nutritional quality during juvenile and sexual development on female resource allocation physiology, life history and courtship behaviour in the cockroach, Nauphoeta cinerea. Nymphs were raised on either a good-quality or poor-quality diet. After adult eclosion, females were either switched to the opposite diet or remained on their original diet. We assessed mating behaviour and lifetime reproductive success for half of the females from each treatment. We evaluated reproductive investment, somatic investment and resource reallocation from reproduction to the soma via oocyte apoptosis in the remaining females. We found that poor juvenile conditions resulted in a fat phenotype with slow juvenile growth and short reproductive lifespan that could not be retrieved with a change in diet. Good juvenile conditions resulted in the converse, but again fixed, phenotype in adulthood. Thus, juvenile nutrition sets adult patterns of resource allocation.     

The Influence of the Early Rearing Environment on the Development of Paternal Care in African Striped Mice

In some biparental mammals, paternal care is important for offspring development and survival. We investigated the influence of the early post‐natal environment on the development of paternal care in the naturally paternal desert‐dwelling African striped mouse (Rhabdomys pumilio). Our aim was to establish whether the expression of paternal care in adult sons is influenced by their experience of paternal care. Offspring were raised in one of three conditions: both parents raised young; mothers raised young alone; and mothers raised young alone but were separated from the father with a barrier. The paternal care behaviour of sons was investigated when they were adults. Contrary to expectations, adult sons raised by the mother alone displayed greater levels of huddling behaviour of their own pups compared to sons raised by both parents. This response appears to be influenced by the early mother–son relationship, because mothers raising pups alone compensated for the absence of fathers by increasing the time spent with pups compared to mothers raising pups with fathers. The mechanisms underpinning the development of paternal care are not apparent in our study. Nonetheless, the development of paternal care is condition‐dependent in male striped mice, indicating that the potential for greater levels of care occurs in the absence of the father and concomitant compensation of maternal care during early development.     

Effects of Emergence Time and Early Social Rearing Environment on Behaviour of Atlantic Salmon: Consequences for Juvenile Fitness and Smolt Migration

Consistent individual differences in behaviour have been well documented in a variety of animal taxa, but surprisingly little is known about the fitness and life-history consequences of such individual variation. In wild salmonids, the timing of fry emergence from gravel spawning nests has been suggested to be coupled with individual behavioural traits. Here, we further investigate the link between timing of spawning nest emergence and behaviour of Atlantic salmon (Salmo salar), test effects of social rearing environment on behavioural traits in fish with different emergence times, and assess whether behavioural traits measured in the laboratory predict growth, survival, and migration status in the wild. Atlantic salmon fry were sorted with respect to emergence time from artificial spawning nest into three groups: early, intermediate, and late. These emergence groups were hatchery-reared separately or in co-culture for four months to test effects of social rearing environment on behavioural traits. Twenty fish from each of the six treatment groups were then subjected to three individual-based behavioural tests: basal locomotor activity, boldness, and escape response. Following behavioural characterization, the fish were released into a near-natural experimental stream. Results showed differences in escape behaviour between emergence groups in a net restraining test, but the social rearing environment did not affect individual behavioural expression. Emergence time and social environment had no significant effects on survival, growth, and migration status in the stream, although migration propensity was 1.4 to 1.9 times higher for early emerging individuals that were reared separately. In addition, despite individuals showing considerable variation in behaviour across treatment groups, this was not translated into differences in growth, survival, and migration status. Hence, our study adds to the view that fitness (i.e., growth and survival) and life-history predictions from laboratory measures of behaviour should be made with caution and ideally tested in nature.     

Effect of temperature on life-history traits and mating calls of a field cricket,Acanthogryllus asiaticus

Ectotherms are sensitive to changes in ambient temperature that impact their physiology and development. To compensate for the effects of variation in temperature, ectotherms exhibit short or long-term physiological plasticity. An extensive body of literature exists towards understanding these effects and the solutions ectotherms have evolved. However, to what extent rearing temperature during early life stages impacts the behaviour expressed in adulthood is less clearly understood. In the present study, we aimed to examine the effects of developmental temperature on life-history traits and mating call features in a tropical field cricket, Acanthogryllus asiaticus. We raised A. asiaticus at two different developmental conditions: 25 °C and 30 °C. We found developmental time and adult lifespan of individuals reared at 30 °C to be shorter than those reared at 25 °C. Increased developmental temperature influenced various body size parameters differentially. Males raised at 30 °C were found to be larger and heavier than those raised at 25 °C, making A. asiaticus an exception to the temperature-size rule. We found a significant effect of change in immediate ambient temperature on different call features of both field-caught and lab-bred individuals. Developmental temperature also affected mating call features wherein individuals raised at higher temperature produced faster calls with a higher peak frequency compared to those raised at lower temperature. In addition, an interactive effect of both developmental and immediate temperature was found on mating call features. Our study highlights the importance of understanding how environmental temperature shapes life-history and sexual communication in crickets.     

A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum)

The maternal behaviour of three species of voles was compared using a semi-naturalistic laboratory system. Meadow vole females spent more time out of the nest, and exhibited less maternal behaviour in terms of nursing and brooding, and more non-social behaviour such as locomoting, eating, and drinking, than the females of the other two species. Across all species, maternal behaviour decreased from parturition onward, while non-social behaviour increased. Paternal care was well developed in the prairie vole and pine vole, but was never observed in the meadow vole. During the first postnatal week, male prairie voles showed a tendency to enter the nest when the female left the young unattended. This trend was not apparent in the male pine vole. The physical parameters of pup development, including eye opening and the development of fur, were similar in all three species. Behavioural development, however, was most rapid in the meadow vole, intermediate in the prairie vole, and slowest in the pine vole. These results are compared with those of previous field and laboratory studies, and are discussed with reference to the life-history strategy of each species.     

Sex differences in the trade-off between feeding and mating in the guppy

Male guppies Poecilia reticulata court almost continuously and often indulge in sneaky mating attempts. Female guppies, on the other hand, devote much of their time to foraging. This paper demonstrates that both sexes reduce their feeding rate in mixed-sex groups relative to single sex ones and suggests that the decrease is less pronounced for females than for males. Thus males make feeding and mating decisions that are dependent on hunger while female foraging behaviour is constrained by sexual harassment. The observed sex differences in behaviour are a consequence of asymmetrical mating costs in males and females.     

Effects of scale on interpreting life-history characteristics of ungulates and carnivores

Many life-history characteristics of large mammals are scale sensitive. We provide examples where varying temporal and spatial scales can affect interpretation of data concerning life-history characteristics in large herbivores and carnivores and offer recommendations for selecting the most appropriate sampling scale or scales. We also document that some animals make decisions concerning their spatial distribution at scales well beyond the size of the home range. Conversely, other decisions involving sexual segregation of sexes, or where to give birth, may be made at scales below the level of the habitat patch. Such differences in behaviour affect our understanding of habitat selection in large herbivores, and interpreting tradeoffs between acquiring essential resources and avoiding predators. Moreover, some landscape attributes may be selected at one scale, whereas other characteristics of the environment may be selected at another. We argue that even sophisticated models for explaining the ecology and behaviour of mammals benefit from framing specific hypotheses that are related to the to the life-history characteristics of those animals. We also believe that the failure to consider and select the most appropriate scale, or suite of scales, may lead to the mismanagement of critical natural resources. We forge relationships among scale, life-history characteristics of mammals, and biodiversity. Finally, we synthesize the literature on scale for large mammals and make recommendations for future research.     

Control of behavioural strategies for capricious environments

In addition to seasonal changes in morphology, physiology and behaviour that occur in predictable annual cycles, there are facultative responses to unpredictable events known as labile (i.e. shortlived) perturbation factors. These rapid behavioural and physiological changes have been termed the ‘emergency life-history stage’ and serve to enhance lifetime fitness. There are four major components: (1) proactive/reactive coping styles for responding to psychosocial stress, predation, and so forth; (2) fight-or-flight responses to rapid emergencies such as an attack by a predator or sudden severe storm; (3) ‘take-it-or-leave-it’ behavioural and physiological responses to longer-term perturbations of the physical environment; and (4) sickness behaviour and fever designed to respond to infection. Glucocorticosteroids interact with cytokines and with other hormones in the hypothalamo-pituitary-adrenal cascade and in the autonomic nervous system to initiate and orchestrate the emergency life-history stage within minutes to hours. Some traits of the emergency life-history stage include: redirection of behaviour from a normal life-history stage to increased foraging, irruptive-type migration during the day, enhanced restfulness at night, elevated gluconeogenesis, and recovery once the perturbation passes. These physiological and behavioural changes allow an individual to avoid potential deleterious effects of stress that may result from chronically elevated levels of circulating glucocorticosteroids over days and weeks. Thus, acute rises in glucocorticosteroids following perturbations of the environment may serve primarily as ‘antistress’ hormones, potentially allowing individuals to avoid chronic stress. Several field studies in diverse habitats indicate that individuals in free-living populations show elevated circulating levels of corticosteroids when they are in an emergency life-history stage. Some simple models based on food availability, body condition, social status and life-history stage, may allow predictions of sensitivity of the hypothalamo-pituitary-adrenal axis to labile perturbation factors. Although there is now extensive evidence for behavioural components of the emergency life-history stage in birds, there remains much to be learned about how other vertebrate groups, especially fish, cope with perturbations of the environment. Because of the unpredictable nature of these perturbations, systematic study of behavioural responses to them is not possible and investigators need to be ‘opportunistic’. There is also a growing need to expand our knowledge of these phenomena because human disturbance, global climate change and pollution are all major perturbations of the environment. How vertebrates respond to the unpredictable in general will thus have important conservation value for the future. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Transgenerational effects on body size caused by early developmental stress in zebra finches

The nutritional and social conditions that individuals experience during early development can have profound effects on their morphology, physiology, behaviour and life history. Experimental increases in brood size in birds can result in reduced offspring condition and survival, indicating that developmental deficits in enlarged broods have negative fitness consequences within the affected generation. To study long-term effects (i.e. transgenerational effects of developmental stress), we conducted a two-step breeding experiment in which we manipulated early developmental conditions in zebra finches Taeniopygia guttata. We raised zebra finches by manipulating brood sizes and controlled for maternal and genetic effects by cross-fostering. In a previous study, we showed that offspring condition and body size decreased with increasing brood size. Here we show that this effect was carried over to the next generation. Body size in nestlings and at nutritional independence was affected by the brood size in which the mothers were raised. Female offspring did significantly worse than male offspring when the mother had been raised in large broods, suggesting a sex-specific influence of maternal effects. These findings link early developmental stress in females with the phenotype of the next generation via maternal effects.     

Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring

Several behavioural effects of prenatal stress are reported in literature, and these seem to depend, among other factors, on the gender studied and the period of gestation in which prenatal stress is applied. In the present study, oral administration of hydrocortisone-acetate (HCA) to 41 pregnant sows was used as a model for prenatal stress, since corticosteroids are considered a key mediator in the effects of prenatal stress. HCA was orally administered to pregnant sows during three periods of gestation: 21-50 (period 1, P1, n = 10), 51-80 (period 2, P2, n = 10) and 81-110 (period 3, P3, n = 10) days after insemination (term 115 days). Control sows (n = 11) received vehicle from 21 to 110 days after insemination. Between days 9 and 48 after birth, treatment effects on male and female piglet behaviour were determined in the home pen and in four different behavioural tests. During the backtest, no gender differences were observed in vocalisations in HCA-piglets, while control males vocalised more than control females. In the home pen at 14 days of age, HCA-piglets spent less time in social interactions than control piglets. During the novel environment test, P1- and P3-piglets walked more than control piglets, but this was not observed during the novel object test, four days later. At weaning, P2- and P3-piglets performed less individual play. Prior to mixing with an unfamiliar piglet (male piglets only), HCA-piglets had lower salivary cortisol concentrations than control piglets, but no difference was observed after mixing. P1-, P2-, and P3- piglets had fewer non-aggressive encounters, and P2-piglets continued fighting longer than control piglets. The present study demonstrates that elevated maternal cortisol concentrations during gestation affect piglet behaviour, and effects do differ between male and female piglets. In addition, effects depend on the period of cortisol administration.     

The ontogeny of courtship, colour and sperm production in male guppies

The onset of sexual behaviour in three age classes of male guppy Poecilia reticulata occurred in synchrony with the appearance of body colouration and anal fin differentiation but not with sperm production. There was also a positive correlation between sperm production and sexual behaviour in the two older age classes.     

Maternal effects on the development of social rank and immunity trade-offs in male laboratory mice (Mus musculus).

Social status in randomly constituted groups of male CFLP mice was predictable from early suckling behaviour and rate of weight gain in natal litters. High-ranking males were those that had suckled on more anterior teats and gained weight more quickly. Rank was not predicted by any measures of sibling interaction or hormone (testosterone, corticosterone) concentration. Aggressiveness in eventual high-rankers was associated negatively with the proportion of males in the litter at birth and the amount of maternal attention received. Aggressive social relationships within natal litters did not predict polarized rank relationships in randomized groups. Nevertheless, while still in their natal litters, and in the absence of aggressive rank relationships, eventual rank categories showed the same difference in modulation of testosterone concentration in relation to current immunocompetence (low-rankers modulating, high-rankers not), as has repeatedly been found in randomized groups by earlier studies. The role of maternal condition in determining rank-related life-history development in male mice is discussed.     

Lekking birds in a tropical forest forego sex for migration

Facultative, partially migratory animals provide a contemporary window into the evolution of migration, offering rare opportunities to examine the life-history trade-offs associated with migration. For the first time, to our knowledge, we describe the nature of these trade-offs, using a lek-breeding tropical bird, the white-ruffed manakin (Corapipo altera). Previous evidence indicated that weather drives post-breeding migration to lower elevations bringing condition-related benefits. Using elevation-sensitive stable isotope measurements and more than 1200 h of behavioural observations, we show that male manakins which migrate incur costs of diminished social status and matings with females the following breeding season. Because migratory tendency depends on inter-annual variation in weather, physical costs of displays and breeding prospects the following year, migratory decisions are subject to both natural and sexual selection, with the outcome of such decisions linked to changing climatic regimes.