Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae

Fecundity-time models of reproductive strategies in marine invertebrates all predict that reproductive success is maximized only at the extreme levels of investment. Selection should drive egg sizes toward small eggs and planktotrophy or large eggs and lecithotrophy. The existence of two distinct larval types, feeding and nonfeeding, has been taken as confirmation of this prediction and has established the current paradigm for larval ecology. However, comparative and experimental evidence does not support the prediction that egg size is minimized in species with planktotrophic larvae. Recent discoveries have documented the existence of planktotrophs that have intermediate egg sizes, differing degrees of dependence on exogenous food, and differing capacities for facultative feeding. A fecundity-time model is presented that includes facultative larval feeding by dissociating the onset of feeding capability from the need for exogenous food. The facultative feeding model shows that reproductive success can be maximized at intermediate levels of investment per offspring between the minimum for development and the threshold for lecithotrophy, depending on the amount of food available to larvae and the intensity of planktonic mortality. A continuum of larval strategies is predicted.     

Examining costs of induced and constitutive immune investment in Tenebrio molitor

Central to the conceptual basis of ecological immunity is the notion that immune effector systems are costly to produce, run, and/or maintain. Using the mealworm beetle, Tenebrio molitor, as a model we investigated two aspects of the costs of innate immunity. We conducted an experiment designed to identify the cost of an induced immune response, and the cost of constitutive investment in immunity, as well as potential interactions. The immune traits under consideration were the encapsulation response and prophylactic cuticular melanization, which are mechanistically linked by the melanin-producing phenoloxidase cascade. If immunity is costly, we predicted reduced longevity and/or fecundity as a consequence of investment in either immune trait. We found a measurable longevity cost associated with producing an inducible immune response (encapsulation). In contrast to other studies, this cost was expressed under ad libitum feeding conditions. We found no measurable costs for constitutive investment in immunity (prophylactic investment in cuticular colour).     

Drivers of age-specific survival in a long-lived seabird: contributions of observed and hidden sources of heterogeneity

1.?We assessed the relative influence of variability in recruitment age, dynamic reproductive investment (time-specific reproductive states) and frailty (unobserved differences in survival abilities across individuals) on survival in the black-legged kittiwake. Furthermore, we examined whether observed variability in survival trajectories was best explained by immediate reproductive investment, cumulative investment, or both. 2.?Individuals that delayed recruitment (≥ age 7) suffered a higher mortality risk than early recruits (age 3), especially later in life, suggesting that recruitment age may be an indicator of individual quality. Although recruitment age helped explain variation in survival, time-varying reproductive investment had a more substantial influence. 3.?The dichotomy of attempting to breed or not explained variability in survival across life better than other parameterizations of reproductive states such as clutch size, brood size or breeding success. In the kittiwake, the sinequanon condition to initiate reproduction is to hold a nest site, which is considered a very competitive activity. This might explain why attempting to breed is the key level of investment that affects survival, independent of the outcome (failure or success). 4.?Interestingly, the more individuals cumulate reproductive attempts over life, the lower their mortality risk, indicating that breeding experience may be a good indicator of parental quality as well. In contrast, attempting to breed at time t increased the risk of mortality between t and t + 1. We thus detected an immediate trade-off between attempting to breed and survival in this population; however, the earlier individuals recruited, and the more breeding experience they accumulated, the smaller the cost. 5.?Lastly, unobserved heterogeneity across individuals improved model fit more (1·3 times) than fixed and dynamic sources of observed heterogeneity in reproductive investment, demonstrating that it is critical to account for both sources of individual heterogeneity when studying survival trajectories. Only after simultaneously accounting for both sources of heterogeneity were we able to detect the 'cost' of immediate reproductive investment on survival and the 'benefit' of cumulative breeding attempts (experience), a proxy to individual quality.     

Testing models of parental investment strategy and offspring size in ants

Parental investment strategies can be fixed or flexible. A fixed strategy predicts making all offspring a single ‘optimal’ size. Dynamic models predict flexible strategies with more than one optimal size of offspring. Patterns in the distribution of offspring sizes may thus reveal the investment strategy. Static strategies should produce normal distributions. Dynamic strategies should often result in non-normal distributions. Furthermore, variance in morphological traits should be positively correlated with the length of developmental time the traits are exposed to environmental influences. Finally, the type of deviation from normality (i.e., skewed left or right, or platykurtic) should be correlated with the average offspring size. To test the latter prediction, we used simulations to detect significant departures from normality and categorize distribution types. Data from three species of ants strongly support the predicted patterns for dynamic parental investment. Offspring size distributions are often significantly non-normal. Traits fixed earlier in development, such as head width, are less variable than final body weight. The type of distribution observed correlates with mean female dry weight. The overall support for a dynamic parental investment model has implications for life history theory. Predicted conflicts over parental effort, sex investment ratios, and reproductive skew in cooperative breeders follow from assumptions of static parental investment strategies and omnipresent resource limitations. By contrast, with flexible investment strategies such conflicts can be either absent or maladaptive. Electronic Supplementary Material Supplementary material is available for this article at     

Dynamic optimization of the sit-to-stand movement

The purpose of this study was to clarify criteria that can predict trajectories during the sit-to-stand movement. In particular, the minimum jerk and minimum torque-change models were examined. Three patterns of sit-to-stand movement from a chair, i.e., upright, natural, and leaning forward, were measured in five young participants using a 3-D motion analysis device (200 Hz). The trajectory of the center of mass and its smoothness were examined, and the optimal trajectories predicted by both models were evaluated. Trajectories of the center of mass predicted by the minimum torque-change model, rather than the minimum jerk model, resembled the measured movements in all rising movement patterns. The upright pattern required greater extension torque of the knee and ankle joints at the instant of seat-off. The leaning-forward pattern required greater extension hip torque and higher movement cost than the natural and upright patterns. These results indicate that the natural sit-to-stand movement might be a result of dynamic optimization.     

Effect of age‐based and environment‐based cues on reproductive investment in Gambusia affinis

We examined the multivariate life‐history trajectories of age 0 and age 1 female Gambusia affinis to determine relative effects of age‐based and environment‐based cues on reproductive investment. Age 0 females decreased reproductive investment prior to the onset of fall and winter months, while age 1 females increased reproductive investment as the summer progressed. The reproductive restraint and terminal investment patterns exhibited by age 0 and age 1 females, respectively, were consistent with the predictions from the cost of reproduction hypothesis. Age 0 females responded to environment‐based cues, decreasing reproductive investment to increase the probability of overwinter survival and subsequent reproductive opportunities in the following summer. Age 1 females responded to age‐based cues, or the proximity of death, increasing investment to current reproduction as future reproductive opportunities decreased late in life. Thus, individuals use multiple cues to determine the level of reproductive investment, and the response to each cue is dependent on the age of an individual.     

Tug-of-war has no borders: it is the missing model in reproductive skew theory

Cooperative breeding often results in unequal reproduction between dominant and subordinate group members. Transactional skew models attempt to predict how unequal reproduction can be before the groups themselves become unstable. A number of variants of transactional models have been developed, with a key difference being whether reproduction is controlled by one party or contested by all. It is shown here that ESS solutions for all situations of contested control over reproduction are given by the original tug-of-war model (TOW). Several interesting results follow. First, TOW can escalate enough to destabilize some types of groups. Particularly vulnerable are those that have low relatedness and gain little from cooperative breeding relative to solitary reproduction. Second, TOW can drastically reduce group productivity and especially the inclusive fitness of dominant individuals. Third, these results contrast strongly with those from variants of TOW models that include concessions to maintain group stability. Such models are shown to be special cases of the general and simpler TOW framework, and to have assumptions that may be biologically suspect. Finally, the overall analysis suggests that there is no mechanism within existing TOW framework that will prevent a costly struggle for reproductive control. Because social species rarely exhibit the high levels of aggression predicted by TOW models, alternative evolutionary mechanisms are considered that can limit conflict and produce more mutually beneficial outcomes. The further development of alternative models to predict patterns of reproductive skew are highly recommended.     

Reproductive effort and costs of reproduction do not explain female-biased sex ratios in the moss Pseudocalliergon trifarium (Amblystegiaceae)

A fundamental assumption in life-history theory is that reproduction is costly. Higher reproductive investment for fruits than for flowers may result in larger costs of reproduction in females than in males, which is often used to explain male-skewed sex ratios in unisexual seed plants. In contrast, bryophytes have predominantly female-biased sex ratios, suggested to be a product of a higher average cost of sexual reproduction in males. Empirical evidence to support this notion is largely lacking. We investigated sex-specific reproductive effort and costs in the unisexual moss Pseudocalliergon trifarium that has a female-dominated expressed sex ratio and rarely produces sporophytes. Annual vegetative segment mass did not differ among male, female, and non-expressing individuals, indicating that there was no threshold-size for sex expression. Mean and annual mass of sexual branches were higher in females than in males, but branch number per segment did not differ between sexes. Prefertilization reproductive effort for females was significantly greater (11.2%) than for males (8.6%). No cost for sexual branch production in terms of reduced relative vegetative growth or decreased investment in reproductive structures in consecutive years was detected. A higher realized reproductive cost in males cannot explain the unbalanced sex ratio in the study species.     

The effect of brain size evolution on feeding propensity,digestive efficiency,and juvenile growth

One key hypothesis in the study of brain size evolution is the expensive tissue hypothesis; the idea that increased investment into the brain should be compensated by decreased investment into other costly organs, for instance the gut. Although the hypothesis is supported by both comparative and experimental evidence, little is known about the potential changes in energetic requirements or digestive traits following such evolutionary shifts in brain and gut size. Organisms may meet the greater metabolic requirements of larger brains despite smaller guts via increased food intake or better digestion. But increased investment in the brain may also hamper somatic growth. To test these hypotheses we here used guppy (Poecilia reticulata) brain size selection lines with a pronounced negative association between brain and gut size and investigated feeding propensity, digestive efficiency (DE), and juvenile growth rate. We did not find any difference in feeding propensity or DE between large‐ and small‐brained individuals. Instead, we found that large‐brained females had slower growth during the first 10 weeks after birth. Our study provides experimental support that investment into larger brains at the expense of gut tissue carries costs that are not necessarily compensated by a more efficient digestive system.     

The impact of dietary restriction, intermittent feeding and compensatory growth on reproductive investment and lifespan in a short-lived fish

While dietary restriction usually increases lifespan, an intermittent feeding regime, where periods of deprivation alternate with times when food is available, has been found to reduce lifespan in some studies but prolong it in others. We suggest that these disparities arise because in some situations lifespan is reduced by the costs of catch-up growth (following the deprivation) and reproductive investment, a factor that has rarely been measured in studies of lifespan. Using three-spined sticklebacks, we show for the first time that while animals subjected to an intermittent feeding regime can grow as large as continuously fed controls that receive the same total amount of food, and can maintain reproductive investment, they have a shorter lifespan. Furthermore, we show that this reduction in lifespan is linked to rapid skeletal growth rate and is due to an increase in the instantaneous risk of mortality rather than in the rate of senescence. By contrast, dietary restriction caused a reduction in reproductive investment in females but no corresponding increase in longevity. This suggests that in short-lived species where reproduction is size dependent, selection pressures may lead to an increase in intrinsic mortality risk when resources are diverted from somatic maintenance to both growth and reproductive investment.     

Fish don't read textbooks: juvenile salmon prove ignorant of foraging theory

The rules governing the selection of feeding patches by foraging animals is an area of intense interest. Much work has focussed on the development of theoretical models that predict when individuals should switch patches. Tests of these models have often been conducted in laboratory environments, but it is not clear how much influence patch‐switching decisions have on population‐level parameters such as growth and distribution in more complex natural environments. We used juvenile Atlantic salmon as a model species to investigate the effects of randomly fluctuating food levels on growth and site selection. We used PIT technology to monitor in detail individuals' patterns of patch use and activity in an artificial stream, at natural densities. This allowed us experimental control of food supplies and sufficient replication, while retaining many features of a natural system. Only a few individuals of high social rank switched patches as predicted by an appropriate foraging model; otherwise, although frequent, patch‐switching was not related to food availability. Thus, while laboratory experiments indicate that this species has the potential to choose foraging sites on the basis of food availability, it is unlikely that this behavioural mechanism is of great importance in natural systems; further tests of foraging models under natural conditions are essential if we are to understand their effects at the level of populations.     

Experimentally activated immune defence in female pied flycatchers results in reduced breeding success

Traditional explanations for the negative fitness consequences of parasitism have focused on the direct pathogenic effects of infectious agents. However, because of the high selection pressure by the parasites, immune defences are likely to be costly and trade off with other fitness-related traits, such as reproductive effort. In a field experiment, we immunized breeding female flycatchers with non-pathogenic antigens (diphtheria-tetanus vaccine), which excluded the direct negative effects of parasites, in order to test the consequences of activated immune defence on hosts' investment in reproduction and self-maintenance. Immunized females decreased their feeding effort and investment in self-maintenance (rectrix regrowth) and had lower reproductive output (fledgling quality and number) than control females injected with saline. Our results reveal the phenotypic cost of immune defence by showing that an activated immune system per se can lower the host's breeding success. This may be caused by an energetic or nutritional trade-off between immune function and physical workload when feeding young or be an adaptive response to 'infection' to avoid physiological disorders such as oxidative stress and immunopathology.     

Male chimpanzees' grooming rates vary by female age, parity, and fertility status

Copulation preferences in our closest living relative, the chimpanzee, suggest that males prefer older females who have had previous offspring. However, this finding is counter to some behavioral models, which predict that chimpanzee males, as promiscuous breeders with minimal costs to mating, should show little or no preference when choosing mating partners (e.g. should mate indiscriminately). To determine if the preferences indicated by copulations appear in other contexts as well as how they interact, we examined how male chimpanzees' grooming patterns varied amongst females. We found that males' preferences were based on interactions among females' fertility status, age, and parity. First, grooming increased with increasing female parity. We further found an effect of the estrous cycle on grooming; when females were at the lowest point of their cycle, males preferentially groomed parous females at peak reproductive age, but during maximal tumescence, males preferred the oldest multiparous females. Nulliparous females received relatively little grooming regardless of age or fertility. Thus, male chimpanzees apparently chose grooming partners based on both female's experience and fertility, possibly indicating a two-pronged social investment strategy. Male selectivity seems to have evolved to effectively distribute costly social resources in a pattern which may increase their overall reproductive success.     

Offspring size-number trade-off in a lizard with small clutch sizes: tests of invariants and potential implications

Models of small clutch sizes predict a number of invariant relationships between means and variances of measures of reproductive investment. However, empirical tests of the models have been lagging behind theoretical work. We tested the predictions using data on the mallee dragon, Ctenophorus fordi, a species where the basic assumptions of the models are likely to be fulfilled. Some, but not all, qualitative predictions of the models were shown to hold true, but the data fitted poorly to quantitative predictions. The patterns of deviation from theory may suggest the presence of a lower, and potentially an upper, limit on egg mass. We also argue that multiple and non-independent allocation decisions between total reproductive effort, growth and maintenance, and offspring size-number allocation could be important factors in the evolution of size-number strategies in lizards and thus need to be taken into account in theoretical models. The present study shows the potential to use small clutch size models to gain further insights into reproductive investment and allocation decisions in squamates.     

Will variation among genetic individuals influence species responses to global climate change?

Increased anthropogenic CO₂ emissions in the last two centuries have lead to rising sea surface temperature and falling ocean pH, and it is predicted that current global trends will worsen over the next few decades. There is limited understanding of how genetic variation among individuals will influence the responses of populations and species to these changes. A microcosm system was set up to study the effects of predicted temperature and CO₂ levels on the bryozoan Celleporella hyalina. In this marine species, colonies grow by the addition of male, female and feeding modular individuals (zooids) and can be physically subdivided to produce a clone of genetically identical colonies. We studied colony growth rate (the addition of zooids), reproductive investment (the ratio of sexual to feeding zooids) and sex ratio (male to female zooids) in four genetically distinct clonal lines. There was a significant effect of clone on growth rate, reproductive investment and sex ratio, with clones showing contrasting responses to the various temperature and pH combinations. Overall, decreasing pH and increasing temperature caused reduction of growth, and eventual cessation of growth was often observed at the highest temperature, especially during the latter half of the 15‐day trials. Reproductive investment increased with increasing temperature and decreasing pH, varying more widely with temperature at the lowest pH. The increased production of males, a general stress response of the bryozoan, was seen upon exposure to reduced pH, but was not expressed at the highest temperature tested, presumably due to the frequent cessation of growth. Further to the significant effect of pH on the measured whole‐colony parameters, observation by scanning electron microscopy revealed surface pitting of the calcified exoskeleton in colonies that were exposed to increased acidity. Studying ecologically relevant processes of growth and reproduction, we demonstrate the existence of relevant levels of variation among genetic individuals which may enable future adaptation via non‐mutational natural selection to falling pH and rising temperature.     

Parental care, cost of reproduction and reproductive skew: a general costly young model

Understanding the mechanisms by which animals resolve conflicts of interest is the key to understanding the basis of cooperation in social species. Conflict over reproductive portioning is the critical type of conflict among cooperative breeders. The costly young model represents an important, but underappreciated, idea about how an individual's intrinsic condition and cost of reproduction should affect the resolution of conflict over the distribution of reproduction within a cooperatively breeding group. However, dominant control in various forms and fixed parental care (offspring fitness dependent solely on total brood size) are assumed in previous versions of costly young models. Here, we develop a general costly young model by relaxing the restrictive assumptions of existing models. Our results show that (1) when the complete-control assumption is relaxed, the costly young model behaves very differently from the original model, and (2) when the fixed parental care assumption is relaxed, the costly young-costly care model displays similar predictions to the tug-of-war model, although the underlying mechanisms causing these similar patterns are different. These results, we believe, help simplify the seemingly divergent predictions of different reproductive skew models and highlight the importance of studying the group members' intrinsic conditions, costs of producing young, and costs of parental care for understanding breeding conflict resolution in cooperatively breeding animals.     

Patterns of reproductive skew in the polygynandrous acorn woodpecker

We compared observed levels of reproductive skew in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus) with those predicted by two alternative transactional models. "Concession" models predict the degree to which parentage is shared assuming that a single dominant is in complete control of reproduction. Alternatively, "restraint" models predict reproductive sharing assuming that the dominant controls only whether subordinates remain in the group but does not control its share of reproduction. Reproductive skew is high among males: on average, the most successful male sires more than three times as many offspring as the next most successful male. Females share parentage equally and have lower constraints on dispersal and lower survival rates compared with males, which is consistent with predictions from the concessions model. Also as predicted by the concessions model, yearly variation in opportunities for dispersal before the breeding season correlates positively with skew. However, in contrast to concessions but consistent with the restraint model, skew decreases with relatedness. Thus, neither model consistently predicts patterns of reproductive skew in this species. We suggest that models of reproductive skew will need to include competitive interactions among potential breeders and mate choice before they will adequately predict patterns of reproductive partitioning in most vertebrate societies.     

Experimental reduction of incubation temperature affects both nestling and adult blue tits Cyanistes caeruleus

Incubation was for a long time considered to be a period of decreased activity and low cost for parents. It was therefore ignored as a potential factor affecting life‐history trade‐offs in birds. Lately this view has started to change, and studies now show that there might be considerable costs connected to incubation. We experimentally reduced the nest temperature during incubation in blue tits Cyanistes caeruleus, thus increasing the energetic cost of incubation, to test the importance of incubation as a component of reproductive costs and for nestling quality. While most other studies use brood size manipulation to manipulate reproductive costs, we were able to separate treatment effects acting during the incubation period from those acting on later reproductive performance by applying a cross‐foster design. We were also able to isolate the effects of decreased incubation temperature on the nestlings from treatment effects acting on incubating females. We found no experimental effect on the length of the incubation period or on hatching success. The lower temperature during incubation, however, caused lower growth rates in nestlings and reduced chick rearing capacity in adults. We conclude that incubation is a costly period, with the potential to affect both the trade‐off between current and future reproduction and the one between parental effort and offspring quality within the current breeding attempt.     

Urban Adolescents' Out-of-School Activity Profiles: Associations with Youth,Family, and School Transition Characteristics

This study applied individual growth trajectory analyses and person-oriented analysis to identify common profiles of out-of-school activity engagement trajectories among racially and ethnically diverse inner city teens (N = 1,430). On average, teens exhibited declining trajectories of participation in school-based and team sports activities and increasing trajectories of religious activity participation. A wide variety of patterns of participation, however, characterized individual teens' involvement across domains. Cluster analysis revealed 10 unique profiles that reflected varying levels of participation in school-based, religious, and team sports activities. Youth demographic characteristics, parental employment status, and school transition timing predicted activity profile membership. Unemployment predicted membership in profiles characterized by low or decreasing activity participation. Later school transitions were associated with membership in high participation profiles.