Repeated assessment of exploration and novelty seeking in the human behavioral pattern monitor in bipolar disorder patients and healthy individuals

Background

Exploration and novelty seeking are cross-species adaptive behaviors that are dysregulated in bipolar disorder (BD) and are critical features of the illness. While these behaviors have been extensively quantified in animals, multivariate human paradigms of exploration are lacking. The human Behavioral Pattern Monitor (hBPM), a human version of the animal open field, identified a signature pattern of hyper-exploration in manic BD patients, but whether exploratory behavior changes with treatment is unknown. The objective of this study was to assess the sensitivity of the hBPM to changes in manic symptoms, a necessary step towards elucidating the neurobiology underlying BD.

Methodology and Principal Findings

Twelve acutely hospitalized manic BD subjects and 21 healthy volunteers were tested in the hBPM over three sessions; all subjects were retested one week after their first session and two weeks after their second session. Motor activity, spatial and entropic (degree of unpredictability) patterns of exploration, and interactions with novel objects were quantified. Manic BD patients demonstrated greater motor activity, extensive and more unpredictable patterns of exploration, and more object interactions than healthy volunteers during all three sessions. Exploration and novelty-seeking slightly decreased in manic BD subjects over the three sessions as their symptoms responded to treatment, but never to the level of healthy volunteers. Among healthy volunteers, exploration did not significantly decrease over time, and hBPM measures were highly correlated between sessions.

Conclusions/Significance

Manic BD patients showed a modest reduction in symptoms yet still demonstrated hyper-exploration and novelty seeking in the hBPM, suggesting that these illness features may be enduring characteristics of BD. Furthermore, behavior in the hBPM is not subject to marked habituation effects. The hBPM can be reliably used in a repeated-measures design to characterize exploration and novelty seeking and, in parallel with animal studies, can contribute to developing treatments that target neuropsychiatric disease.     

Learning rate and temperament in a high predation risk environment

Living in challenging environments can influence the behavior of animals in a number of ways. For instance, populations of prey fish that experience frequent, nonlethal interactions with predators have a high proportion of individuals that express greater reaction to risk and increased activity and exploration—collectively known as temperament traits. Temperament traits are often correlated, such that individuals that are risk-prone also tend to be active and explore more. Spatial learning, which requires the integration of many sensory cues, has also been shown to vary in fish exposed to different levels of predation threat. Fish from areas of low predation risk learn to solve spatial tasks faster than fish from high predation areas. However, it is not yet known whether simpler forms of learning, such as learning associations between two events, are similarly influenced. Simple forms of associative learning are likely to be affected by temperament because a willingness to approach and explore novel situations could provide animals with a learning advantage. However, it is possible that routine-forming and inflexible traits associated with risk-prone and increased exploratory behavior may act in the opposite way and make risk-prone individuals poorer at learning associations. To investigate this, we measured temperament in Panamanian bishop fish (Brachyrhaphis episcopi) sampled from a site known to contain many predators. The B. episcopi were then tested with an associative learning task. Within this population, fish that explored more were faster at learning a cue that predicted access to food, indicating a link between temperament and basic learning abilities.     

Aggression and peripheralization in subadult male long-tailed macaques in Singapore

Aggression and peripheralization between adult and subadult male macaques have been postulated as proximate causes for dispersal, but empirical evidence for this relationship is scarce. To investigate the level of aggression and peripheralization experienced by subadult males, we conducted focal animal and scan sampling of two long-tailed macaque (Macaca fascicularis) groups in the highly anthropogenic environment of Singapore’s Central Nature Reserve. We followed two subadult males each in two groups and compared (1) aggression between subadult and adult males and (2) peripheralization measured by (a) greater interindividual distances, (b) more noninteractive behaviors, and (c) fewer interactive behaviors. After 72 focal hours, results suggest varying levels of peripheralization and consistently low levels of aggression among all four males. Data herein call into question the role of aggression in intragroup interactions. Differences in affiliation patterns appear to be core factors in determining the individual degree of peripheralization. Ultimately, strategic choices related to an individual’s place within the natal group (e.g., affiliations, rank of relatives) may be important to cost–benefit assessments; these choices have significant implications in both the short term (i.e., dispersal timing) and long term (i.e., reproductive success). This study is a first step toward understanding macaque behavior in anthropogenic environments; further exploration is needed to anticipate how landscape changes might influence macaque dispersal patterns. Greater understanding will come from recognition that social mechanisms are highly individualized and constantly dynamic, especially for highly cognitive, social species, and in ever increasingly dynamic anthropogenic environments.     

Is exploration a metric for information gathering? Attraction to novelty and plasticity in black-capped chickadees

Animals can learn about the value of resources and predation risk by exploring novel environments or exploring novel stimuli in their regular environments. Still, there is a disconnect in the way that exploration has been defined and measured; exploration is defined in terms of information acquisition, while measured in terms of movement speed and diversity of contacted items in a novel environment. If exploration is indeed a measurement of information gathering, fast explorers should seek to reduce uncertainty about their environment more than slow explorers. Exploration speed has also been linked to behavioral plasticity, where fast explorers move fast but collect less detailed information, thereby forming routines and expressing less plasticity than slow explorers. We test these two hypotheses by comparing exploration in a novel environment to individuals' attraction to novelty and behavioral plasticity. Our results support the view that exploration is a measurement of information-gathering tendencies as fast explorers were more likely to collect novel information, which should reduce uncertainty further than sampling familiar information sources, compared with slower explorers. Furthermore, faster explorers switched to sampling novel information more quickly than slow explorers when the value of the familiar option decreased, opposing the widely held view that faster explorers present more routine-like behavior. By providing familiar and novel foraging options in close spatial contiguity, we demonstrate an attraction to novelty in faster explorers that cannot be confounded by activity rate, thereby suggesting that these individuals seek to reduce uncertainty. In conclusion, our results support the biological validity of the term “exploration” through its association with information gathering.     

Trojan Genes and Transparent Genomes: Sexual Selection,Regulatory Evolution and the Real Hopeful Monsters

Potential impacts of genetically modified (GM) animals in natural environments are explored in a framework of regulatory evolution. Transgenic growth hormone animals express remarkable alterations and plasticity in development, physiology and behavior in response to environmental factors (nutrition, temperature, photoperiod), suggesting that standard laboratory assessments are likely to underestimate their evolutionary potential. Sexual selection is examined in the context of female self-referent appraisal of male fitness that reflects performance in the species-specific niche. Wild-type females may recognize and discriminate against GM males (the Transparent Genome Hypothesis) but if accepted as mates, pleiotropic disruption associated with GMs may reduce fitness of the natural population (the Trojan Gene Hypothesis). Alternatively, facilitation of regulatory evolution by sexual reproduction (recombination and segregation) may derive modifier selection, masking, integration, or niche shifts. Other aspects explored include mutation theory, purging, pleiotropy, epigenetics and plasticity, behavior and the Bruce effect, and mismatch of genetic or epigenetic background between GM stock and natural populations.     

A symbiotic brain-machine interface through value-based decision making

Background

In the development of Brain Machine Interfaces (BMIs), there is a great need to enable users to interact with changing environments during the activities of daily life. It is expected that the number and scope of the learning tasks encountered during interaction with the environment as well as the pattern of brain activity will vary over time. These conditions, in addition to neural reorganization, pose a challenge to decoding neural commands for BMIs. We have developed a new BMI framework in which a computational agent symbiotically decoded users'' intended actions by utilizing both motor commands and goal information directly from the brain through a continuous Perception-Action-Reward Cycle (PARC).

Methodology

The control architecture designed was based on Actor-Critic learning, which is a PARC-based reinforcement learning method. Our neurophysiology studies in rat models suggested that Nucleus Accumbens (NAcc) contained a rich representation of goal information in terms of predicting the probability of earning reward and it could be translated into an evaluative feedback for adaptation of the decoder with high precision. Simulated neural control experiments showed that the system was able to maintain high performance in decoding neural motor commands during novel tasks or in the presence of reorganization in the neural input. We then implanted a dual micro-wire array in the primary motor cortex (M1) and the NAcc of rat brain and implemented a full closed-loop system in which robot actions were decoded from the single unit activity in M1 based on an evaluative feedback that was estimated from NAcc.

Conclusions

Our results suggest that adapting the BMI decoder with an evaluative feedback that is directly extracted from the brain is a possible solution to the problem of operating BMIs in changing environments with dynamic neural signals. During closed-loop control, the agent was able to solve a reaching task by capturing the action and reward interdependency in the brain.     

Galantamine reverses scopolamine-induced behavioral alterations in Dugesia tigrina

In planaria (Dugesia tigrina), scopolamine, a nonselective muscarinic receptor antagonist, induced distinct behaviors of attenuated motility and C-like hyperactivity. Planarian locomotor velocity (pLMV) displayed a dose-dependent negative correlation with scopolamine concentrations from 0.001 to 1.0 mM, and a further increase in scopolamine concentration to 2.25 mM did not further decrease pLMV. Planarian hyperactivity counts was dose-dependently increased following pretreatment with scopolamine concentrations from 0.001 to 0.5 mM and then decreased for scopolamine concentrations ≥1 mM. Planarian learning and memory investigated using classical Pavlovian conditioning experiments demonstrated that scopolamine (1 mM) negatively influenced associative learning indicated by a significant decrease in % positive behaviors from 86 % (control) to 14 % (1 mM scopolamine) and similarly altered memory retention, which is indicated by a decrease in % positive behaviors from 69 % (control) to 27 % (1 mM scopolamine). Galantamine demonstrated a complex behavior in planarian motility experiments since co-application of low concentrations of galantamine (0.001 and 0.01 mM) protected planaria against 1 mM scopolamine-induced motility impairments; however, pLMV was significantly decreased when planaria were tested in the presence of 0.1 mM galantamine alone. Effects of co-treatment of scopolamine and galantamine on memory retention in planaria via classical Pavlovian conditioning experiments showed that galantamine (0.01 mM) partially reversed scopolamine (1 mM)-induced memory deficits in planaria as the % positive behaviors increased from 27 to 63 %. The results demonstrate, for the first time in planaria, scopolamine’s effects in causing learning and memory impairments and galantamine’s ability in reversing scopolamine-induced memory impairments.     

Novelty is not surprise: Human exploratory and adaptive behavior in sequential decision-making

Classic reinforcement learning (RL) theories cannot explain human behavior in the absence of external reward or when the environment changes. Here, we employ a deep sequential decision-making paradigm with sparse reward and abrupt environmental changes. To explain the behavior of human participants in these environments, we show that RL theories need to include surprise and novelty, each with a distinct role. While novelty drives exploration before the first encounter of a reward, surprise increases the rate of learning of a world-model as well as of model-free action-values. Even though the world-model is available for model-based RL, we find that human decisions are dominated by model-free action choices. The world-model is only marginally used for planning, but it is important to detect surprising events. Our theory predicts human action choices with high probability and allows us to dissociate surprise, novelty, and reward in EEG signals.     

HNCA+, HNCO+, and HNCACB+ experiments: improved performance by simultaneous detection of orthogonal coherence transfer pathways

Three experiments, BEST–TROSY HNCA+, HNCO+ and HNCACB+ are presented for sequential backbone resonance assignment of ¹³C, ¹⁵N labelled proteins. The novelty of these experiments with respect to conventional pulse sequences is the detection of additional orthogonal coherence transfer pathways that results in enhanced sensitivity for sequential correlations without significantly compromising the intensity of intra-residue correlation peaks. In addition, a 2-step phase cycle separates peaks originating from the orthogonal coherence transfer pathways in 2 sub-spectra, thus providing similar information as obtained from performing a pair of sequential and intra-residue correlation experiments.     

Biological modeling of complex chemotaxis behaviors for C. elegans under speed regulation—a dynamic neural networks approach

In this paper, the modeling of several complex chemotaxis behaviors of C. elegans is explored, which include food attraction, toxin avoidance, and locomotion speed regulation. We first model the chemotaxis behaviors of food attraction and toxin avoidance separately. Then, an integrated chemotaxis behavioral model is proposed, which performs the two chemotaxis behaviors simultaneously. The novelty and the uniqueness of the proposed chemotaxis behavioral models are characterized by several attributes. First, all the chemotaxis behavioral model sare on biological basis, namely, the proposed chemotaxis behavior models are constructed by extracting the neural wire diagram from sensory neurons to motor neurons, where sensory neurons are specific for chemotaxis behaviors. Second, the chemotaxis behavioral models are able to perform turning and speed regulation. Third, chemotaxis behaviors are characterized by a set of switching logic functions that decide the orientation and speed. All models are implemented using dynamic neural networks (DNN) and trained using the real time recurrent learning (RTRL) algorithm. By incorporating a speed regulation mechanism, C. elegans can stop spontaneously when approaching food source or leaving away from toxin. The testing results and the comparison with experiment results verify that the proposed chemotaxis behavioral models can well mimic the chemotaxis behaviors of C. elegans in different environments.     

FastMPJ: a scalable and efficient Java message-passing library

The performance and scalability of communications are key for high performance computing (HPC) applications in the current multi-core era. Despite the significant benefits (e.g., productivity, portability, multithreading) of Java for parallel programming, its poor communications support has hindered its adoption in the HPC community. This paper presents FastMPJ, an efficient message-passing in Java (MPJ) library, boosting Java for HPC by: (1) providing high-performance shared memory communications using Java threads; (2) taking full advantage of high-speed cluster networks (e.g., InfiniBand) to provide low-latency and high bandwidth communications; (3) including a scalable collective library with topology aware primitives, automatically selected at runtime; (4) avoiding Java data buffering overheads through zero-copy protocols; and (5) implementing the most widely extended MPI-like Java bindings for a highly productive development. The comprehensive performance evaluation on representative testbeds (InfiniBand, 10 Gigabit Ethernet, Myrinet, and shared memory systems) has shown that FastMPJ communication primitives rival native MPI implementations, significantly improving the efficiency and scalability of Java HPC parallel applications.     

Self-aggression in macaques: Five case studies

Spontaneous self-aggressive behaviors were observed in five adult male rhesus monkeys (Macaca mulatta) housed at a university facility. All were individually caged, were free of intercurrent disease, and were being utilized in ongoing research studies. The self-aggressive behaviors observed included self-biting, self-clasping, self-slapping, self-rubbing and threatening of body parts. In several cases, wounds were inflicted and medical treatment was required due to the severity of the lesions. A review of the animals' clinical histories revealed an increased level of self-aggressive behavior in four of five monkeys during such stressful or stimulating conditions as movement of the animal to a new cage, movement of animals out of the room or escape of other monkeys from their cages. The frequency with which these behaviors occurred was quantitated experimentally. The results revealed an increased level of self-aggressive behavior in two of these animals during the videotaped sessions in response to aggressive contacts with the investigator. In contrast, one monkey exhibited self-aggressive behavior both clinically and experimentally in the absence of environmental stimuli or human contact. Clinical management of self-aggressive monkeys included housing monkeys only with physically smaller primates, decreasing the level of environmental stimuli, and drug therapy. Haloperidol was used with success in one animal that exhibited severe self-aggressive behavior.     

A New Record of a Host-Parasitoid Interaction: Hymenoepimecis veranii Lofredo & Penteado-Dias, 2009 (Hymenoptera: Ichneumonidae) Parasitizing Araneus orgaos Levi, 1991 (Araneae: Araneidae)

The genus Hymenoepimecis only occurs in the Neotropics. In some species of this genus, the larval stage modifies the behavior of the spider hosts, inducing then to construct a modified web. The wasp Hymenoepimecis veranii has been previously described as an ectoparasitoid of the spider Araneus omnicolor. This study provides detailed information about the natural history of the host-parasitoid interaction involving this wasp with a new host, the spider Araneus orgaos (Araneae: Araneidae), which occurs sympatrically with A. omnicolor.     

The Effect of an Acute Bout of Moderate-Intensity Aerobic Exercise on Motor Learning of a Continuous Tracking Task

Introduction

There is evidence for beneficial effects of acute and long-term exercise interventions on several forms of memory, including procedural motor learning. In the present study we examined how performing a single bout of continuous moderate intensity aerobic exercise would impact motor skill acquisition and retention in young healthy adults, compared to a period of rest. We hypothesized that exercise would improve motor skill acquisition and retention, compared to motor practice alone.

Materials and Methods

Sixteen healthy adults completed sessions of aerobic exercise or seated rest that were immediately followed by practice of a novel motor task (practice). Exercise consisted of 30 minutes of continuous cycling at 60% peak O₂ uptake. Twenty-four hours after practice, we assessed motor learning with a no-exercise retention test (retention). We also quantified changes in offline motor memory consolidation, which occurred between practice and retention (offline). Tracking error was separated into indices of temporal precision and spatial accuracy.

Results

There were no differences between conditions in the timing of movements during practice (p = 0.066), at retention (p = 0.761), or offline (p = 0.966). However, the exercise condition enabled participants to maintain spatial accuracy during practice (p = 0.477); whereas, following rest performance diminished (p = 0.050). There were no significant differences between conditions at retention (p = 0.532) or offline (p = 0.246).

Discussion

An acute bout of moderate-intensity aerobic exercise facilitated the maintenance of motor performance during skill acquisition, but did not influence motor learning. Given past work showing that pairing high intensity exercise with skilled motor practice benefits learning, it seems plausible that intensity is a key modulator of the effects of acute aerobic exercise on changes in complex motor behavior. Further work is necessary to establish a dose-response relationship between aerobic exercise and motor learning.     

The relationship between DRD4 polymorphisms and phenotypic correlations of behaviors in the collared flycatcher

There is increasing evidence that the genetic architecture of exploration behavior includes the dopamine receptor D4 gene (DRD4). Such a link implies that the within‐individual consistency in the same behavior has a genetic basis. Behavioral consistency is also prevalent in the form of between‐individual correlation of functionally different behaviors; thus, the relationship between DRD4 polymorphism and exploration may also be manifested for other behaviors. Here, in a Hungarian population of the collared flycatcher, Ficedula albicollis, we investigate how males with distinct DRD4 genotypes differ in the consistent elements of their behavioral displays during the courtship period. In completely natural conditions, we assayed novelty avoidance, aggression and risk‐taking, traits that were previously shown repeatable over time and correlate with each other, suggesting that they could have a common mechanistic basis. We identified two single‐nucleotide polymorphisms (SNP554 and SNP764) in the exon 3 of the DRD4 gene by sequencing a subsample, then we screened 202 individuals of both sexes for these SNPs. Focusing on the genotypic variation in courting males, we found that “AC” heterozygote individuals at the SNP764 take lower risk than the most common “AA” homozygotes (the “CC” homozygotes were not represented in our subsample of males). We also found a considerable effect size for the relationship between SNP554 polymorphism and novelty avoidance. Therefore, in addition to exploration, DRD4 polymorphisms may also be associated with the regulation of behaviors that may incur fear or stress. Moreover, polymorphisms at the two SNPs were not independent indicating a potential role for genetic constraints or another functional link, which may partially explain behavioral correlations.     

Motor learning with unstable neural representations

It is often assumed that learning takes place by changing an otherwise stable neural representation. To test this assumption, we studied changes in the directional tuning of primate motor cortical neurons during reaching movements performed in familiar and novel environments. During the familiar task, tuning curves exhibited slow random drift. During learning of the novel task, random drift was accompanied by systematic shifts of tuning curves. Our analysis suggests that motor learning is based on a surprisingly unstable neural representation. To explain these results, we propose that motor cortex is a redundant neural network, i.e., any single behavior can be realized by multiple configurations of synaptic strengths. We further hypothesize that synaptic modifications underlying learning contain a random component, which causes wandering among synaptic configurations with equivalent behaviors but different neural representations. We use a simple model to explore the implications of these assumptions.     

Activity and impulsive action are controlled by different genetic and environmental factors

Both impulsivity in operant tasks and locomotor activity in a novel open field are known to predict the development of addiction-related behavior in rodents. In this study, we investigated to what extent impulsivity in the five-choice serial reaction time task and various measures of novelty exploration are controlled by shared genetic and environmental factors in 12 different inbred mouse strains. No genetic correlation was observed between the level of impulsivity and levels of activity, a low correlation was observed with traditional measures of anxiety-like behavior (impulsive strains tend to be less anxious) and a highly significant correlation was found between impulsivity and specific aspects of movement. Furthermore, we found that impulsivity and all measures of novelty exploration were under control of different environmental factors. Interestingly, in the dorsal medial prefrontal cortex, a brain region involved in impulsivity and activity in novelty exploration tests; these behavioral measures correlated with the expression of different genes (respectively, Frzb , Snx5, BC056474 and the previously identified Glo1 ). Taken together, our study shows that impulsivity and activity in novelty exploration tests are genetically and environmentally distinct, suggesting that mouse models of these behaviors provide complementary insights into the development of substance abuse disorder.     

High Fungal Diversity and Abundance Recovered in the Deep-Sea Sediments of the Pacific Ocean

Knowledge about the presence and ecological significance of bacteria and archaea in the deep-sea environments has been well recognized, but the eukaryotic microorganisms, such as fungi, have rarely been reported. The present study investigated the composition and abundance of fungal community in the deep-sea sediments of the Pacific Ocean. In this study, a total of 1,947 internal transcribed spacer (ITS) regions of fungal rRNA gene clones were recovered from five sediment samples at the Pacific Ocean (water depths ranging from 5,017 to 6,986 m) using three different PCR primer sets. There were 16, 17, and 15 different operational taxonomic units (OTUs) identified from fungal-universal, Ascomycota-, and Basidiomycota-specific clone libraries, respectively. Majority of the recovered sequences belonged to diverse phylotypes of Ascomycota (25 phylotypes) and Basidiomycota (18 phylotypes). The multiple primer approach totally recovered 27 phylotypes which showed low similarities (≤97 %) with available fungal sequences in the GenBank, suggesting possible new fungal taxa occurring in the deep-sea environments or belonging to taxa not represented in the GenBank. Our results also recovered high fungal LSU rRNA gene copy numbers (3.52?×?10⁶ to 5.23?×?10⁷copies/g wet sediment) from the Pacific Ocean sediment samples, suggesting that the fungi might be involved in important ecological functions in the deep-sea environments.     

Ghrelin Influences Novelty Seeking Behavior in Rodents and Men

Recent discoveries indicate an important role for ghrelin in drug and alcohol reward and an ability of ghrelin to regulate mesolimbic dopamine activity. The role of dopamine in novelty seeking, and the association between this trait and drug and alcohol abuse, led us to hypothesize that ghrelin may influence novelty seeking behavior. To test this possibility we applied several complementary rodent models of novelty seeking behavior, i.e. inescapable novelty-induced locomotor activity (NILA), novelty-induced place preference and novel object exploration, in rats subjected to acute ghrelin receptor (growth hormone secretagogue receptor; GHSR) stimulation or blockade. Furthermore we assessed the possible association between polymorphisms in the genes encoding ghrelin and GHSR and novelty seeking behavior in humans. The rodent studies indicate an important role for ghrelin in a wide range of novelty seeking behaviors. Ghrelin-injected rats exhibited a higher preference for a novel environment and increased novel object exploration. Conversely, those with GHSR blockade drastically reduced their preference for a novel environment and displayed decreased NILA. Importantly, the mesolimbic ventral tegmental area selective GHSR blockade was sufficient to reduce the NILA response indicating that the mesolimbic GHSRs might play an important role in the observed novelty responses. Moreover, in untreated animals, a striking positive correlation between NILA and sucrose reward behavior was detected. Two GHSR single nucleotide polymorphisms (SNPs), rs2948694 and rs495225, were significantly associated with the personality trait novelty seeking, as assessed using the Temperament and Character Inventory (TCI), in human subjects. This study provides the first evidence for a role of ghrelin in novelty seeking behavior in animals and humans, and also points to an association between food reward and novelty seeking in rodents.     

Antagonistic Parent-Offspring Co-Adaptation

Background

In species across taxa, offspring have means to influence parental investment (PI). PI thus evolves as an interacting phenotype and indirect genetic effects may strongly affect the co-evolutionary dynamics of offspring and parental behaviors. Evolutionary theory focused on explaining how exaggerated offspring solicitation can be understood as resolution of parent-offspring conflict, but the evolutionary origin and diversification of different forms of family interactions remains unclear.

Methodology/Principal Findings

In contrast to previous theory that largely uses a static approach to predict how “offspring individuals” and “parental individuals” should interact given conflict over PI, we present a dynamic theoretical framework of antagonistic selection on the PI individuals obtain/take as offspring and the PI they provide as parents to maximize individual lifetime reproductive success; we analyze a deterministic and a stochastic version of this dynamic framework. We show that a zone for equivalent co-adaptation outcomes exists in which stable levels of PI can evolve and be maintained despite fast strategy transitions and ongoing co-evolutionary dynamics. Under antagonistic co-adaptation, cost-free solicitation can evolve as an adaptation to emerging preferences in parents.

Conclusions/Significance

We show that antagonistic selection across the offspring and parental life-stage of individuals favors co-adapted offspring and parental behavior within a zone of equivalent outcomes. This antagonistic parent-offspring co-adaptation does not require solicitation to be costly, allows for rapid divergence and evolutionary novelty and potentially explains the origin and diversification of the observed provisioning forms in family life.