Lifespan varies widely among individuals, yet the extent to which such variation persists when genetic and environmental differences are minimized remains unclear. Here we quantify such stochastic lifespan variation in a naturally clonal vertebrate and test whether and how this variation is linked to early-life behavioral individuality. We followed N = 33 genetically identical Amazon mollies ( Poecilia formosa ), separated on day 1 of their life into highly standardized environments, from birth to death. Despite genetic uniformity and environmental standardization, lifespan varies markedly, spanning 502 – 826 days. Continuous high-resolution behavioral tracking during the first four weeks of life reveals that seemingly stochastic early-life activity differences explain 32.5% of this variation. Higher activity predicts shorter lifespan during the first two weeks, but as activity levels and among-individual variation in activity decline over early development, a U-shaped relationship emerges, with both low- and high-activity individuals outliving those with intermediate activity. These findings show that signatures of lifespan emerge within days of birth, even among genetically identical individuals, highlighting developmental stochasticity and early-life contingencies as major contributors to variation in life-history outcomes.

Behaviors – and thus behavioral individuality – rarely emerge fully formed but are instead built gradually through development, shaped by processes involving learning, skill formation, and experience. Prevailing theory in behavioral ecology, however, has largely focused on static equilibrium outcomes where behaviors are analyzed only as fully formed traits, often neglecting development. Here, we challenge this tradition by placing gradual development at the center of the emergence of individuality. We show, using a hierarchy of models, that when traits develop incrementally and are subject to even minimal stochasticity, individuality is not a special case but an inevitable outcome. Early chance deviations are preserved and amplified by the path-dependent nature of development, generating high and sustained repeatability across individuals. We demonstrate that this logic holds across neutral processes, directional development toward phenotypic targets, and adaptive, state-dependent decision-making. By integrating stochasticity, developmental dynamics, and optimality theory, our results recast individuality as a generic property of gradual development, not requiring specific adaptive or constraint-based explanations. More broadly, our findings illustrate that understanding biological variation may often require a shift away from static equilibria thinking toward explicitly time-dependent, developmental perspectives.

ABSTRACT The study of among-individual phenotypic variation arising in the apparent absence of genetic and environmental differences has recently emerged as a rapidly growing research area. Despite growing recognition of its existence and fitness relevance, it remains unknown whether signatures of such presumably stochastically induced variation can be transmitted across generations. To address this knowledge gap, we performed a two-generation behavioral screening with a naturally clonal fish: 34 genetically identical mothers and their 232 offspring were separated after birth into near-identical environments, with early-life behavior being tracked continuously at high resolution, constituting a total of ∼19,000 observation hours. We find consistent among-individual differences in behavior (i.e., activity and feeding patterns) in both mothers and offspring. Mother behavior correlates with offspring activity (but not offspring feeding): mothers that spend more time feeding produce more active offspring. We find no evidence of body size (maternal or offspring) mediating mother-offspring behavioral associations. Our study provides first evidence for the non-genetic transmission of among-individual phenotypic differences that arise in the apparent absence of genetic or environmental differences, highlighting the potential importance of this variation for evolutionary processes and the adaptive potential of populations.

Paternal effects, i.e., effects of fathers on the phenotype of their offspring that are not mediated by the transmission of alleles, are increasingly recognized as a potentially significant source of phenotypic variation across taxa - even in the absence of paternal care. Gynogenetic systems, which rely on sperm to trigger embryogenesis without incorporating male genetic material, provide a powerful way to experimentally isolate paternal effects from effects caused by the integration of male genetic material. Up to now, however, paternal effects remain largely unexplored in these systems. Here, we tested for non-genetic paternal effects in the gynogenetic Amazon molly (Poecilia formosa): a naturally clonal, all-female species with no parental care. Using a highly controlled breeding experiment involving 60 Atlantic molly males (Poecilia mexicana) and 54 Amazon molly females from a single clonal lineage, we generated 128 broods and 2,435 offspring. While males were drawn from a naturally variable stock population, females - next to being genetically identical - were standardized for age, size, descent, and developmental experience. We asked whether male identity or body size predicted offspring size - a key offspring phenotypic trait. We also asked whether male identity or body size predicted brood size. Male identity explained either no or only very small proportions of the variation in offspring or brood size. Larger males were weakly associated with larger offspring, but this effect was minimal (partial R2 ~ 1.5%). However, these patterns did not hold consistently across all data exclusion criteria and analytical variants, underscoring their tentative nature and highlighting the need for further investigation. Our study offers one of the first empirical tests of male effects in a gynogenetic vertebrate, providing valuable quantitative benchmarks for the magnitude of such effects in gynogenetic systems.

Studies on collective cognition provide many examples of how the efficient spread of information within groups leads to benefits with increasing group size. However, little is known if groups also amplify maladaptive information such as false alarms and whether such costs reduce possible benefits. Here, we investigated wild fish shoals responding collectively with escape dives when attacked by birds. We analyzed the collective response in reaction to bird attacks and similar but harmless flybys as a function of shoal size. Larger shoals increasingly detected predator attacks (i.e., true positives), while their response facing harmless flybys (i.e., false alarms) remained constant. Furthermore, decision time decreased with increasing shoal size. Larger shoals were thus able to simultaneously overcome two major trade-offs inherent in solitary decision-making: the trade-off between true and false positives and the trade-off between speed and accuracy. Our findings set the stage for the next generation of studies investigating the mechanisms underlying collective decision-making.

Developmental plasticity at the behavioral repertoire level allows animals to incrementally adjust their behavioral phenotypes to match their environments through ontogeny. Quantifying this plasticity in sufficient resolution across substantial periods of development, however, has been challenging. Here, we use high-resolution tracking to monitor 45 genetically identical Amazon mollies (Poecilia formosa) reared in near-identical environments over their first four weeks of life. We analyze behavior at 0.2-s resolution to assess plasticity across entire behavioral repertoires. Testing a key prediction from Bayesian models-that plasticity should decline in stable environments-we measure plasticity using both individual behavioral metrics and a bespoke "behavioral entropy" approach in a multi-dimensional phenotype space. Surprisingly, and despite closely conforming to model assumptions, we find a consistent initial two-week increase in movement plasticity before a decline. These results challenge expectations about how plasticity unfolds early in life and highlight the importance of continuous behavioral tracking for evaluating developmental theories.

Paternal effects, i.e., effects of males on the phenotypes of their offspring that are not caused by the integration of male genetic material, are increasingly recognized as a potentially significant source of phenotypic variation across taxa - even in the absence of paternal care. Gynogenetic systems, which rely on sperm to trigger embryogenesis without incorporating male genetic material, provide a powerful way to experimentally isolate potential paternal effects from effects caused by the integration of male genetic material; up to now, however, paternal effects remain largely unexplored in these systems. Here, we test for paternal effects in the gynogenetic Amazon molly ( Poecilia formosa ): a naturally clonal, all-female species with no parental care. Using a highly controlled breeding experiment involving 59 Atlantic molly males ( P. mexicana ) and 57 Amazon molly females, we generated 169 broods and 2,966 offspring. While males were drawn from a naturally variable stock population, females – next to being genetically identical – were highly standardized for age, size, descent, and developmental experience. We asked whether male identity or body size predicted offspring size – a key offspring phenotypic trait. We also asked whether male identity or body size predicted brood size. While we found substantial variation in both offspring size and brood size, we found no evidence for paternal effects on either trait. Next to providing an experimental test for paternal effects in a gynogenetic system, our results also strengthen the Amazon molly’s status as a model species for studying – in a highly controlled fashion – the developmental emergence of phenotypic variation. ### Competing Interest Statement The authors have declared no competing interest.

Predation risk is one of the most important factors generating behavioral differences among populations. In addition, recent attention focusses on predation as a potential driver of patterns of individual behavioral variation within prey populations. Previous studies provide mixed results, reporting either increased or decreased among-individual variation in response to risk. Here, we take an explicit developmental approach to documenting how among-individual variation develops over time in response to predator exposure, controlling for both genetic and experiential differences among individuals. We reared juveniles of naturally clonal Amazon mollies, Poecilia formosa, either with or without a predator visible during feedings over 4 weeks and analyzed activity during feedings, time spent feeding and number of visits to the feeding spot. (I) Predator-exposed fish did not differ from control fish in average feeding behavior, but they were less active during feeding trials. (II) In the absence of the predator, substantial changes in among-individual variation over time were detected: among-individual differences in feeding duration increased whereas differences in activity decreased, but there were no changes in feeder visits. In contrast, in the presence of a predator, among-individual variation in all three behaviors was stable over time and often lower compared to control conditions. Our work suggests that predation risk may have an overall stabilizing effect on the development of individual variation and that differences in predation risk may well lead to population-wide differences in among-individual behavioral variation.

Studies on collective cognition have provided many examples of decision-making benefits in terms of animals sharing information about predators, prey or resources in their environment. It has been shown how the efficient spread of adaptive information within groups can pro-vide benefits which increase with group size. Little is known, however, to which extent groups also amplify maladaptive information such as false alarms and whether such costs reduce or even nullify the above benefits. Here, we investigated fish shoals in the wild that responded collectively with escape dives when attacked by birds. We analysed the response of shoals in reaction to hard-to-detect bird attacks and similar but harmless flybys as a func-tion of shoal size. With increasing shoal size fish increasingly detected predator attacks (true positives) while their false alarms remained constant. Therefore, larger shoals became better at correctly classifying potentially dangerous stimuli rather than becoming more sensitive to all stimuli potentially related to attacks. In addition, decision time decreased with increasing shoal size. Larger shoals were thus able to mitigate two major trade-offs inherent in solitary decision making: the trade-off between true and false positives and the trade-off between speed and accuracy. We report performance increases at shoal sizes of tens of thousands of fish and pose challenges for the modelling of the underlying mechanisms. ### Competing Interest Statement The authors have declared no competing interest.

Recent studies have documented among-individual phenotypic variation that emerges in the absence of apparent genetic and environmental differences, but it remains an open question whether such seemingly stochastic variation has fitness consequences. We perform a life-history experiment with naturally clonal fish, separated directly after birth into near-identical (i.e., highly standardized) environments, quantifying 2522 offspring from 152 broods over 280 days. We find that (i) individuals differ consistently in the size of offspring and broods produced over consecutive broods, (ii) these differences are observed even when controlling for trade-offs between brood size, offspring size and reproductive onset, indicating individual differences in life-history productivity and (iii) early-life behavioral individuality in activity and feeding patterns, with among-individual differences in feeding being predictive of growth, and consequently offspring size. Thus, our study provides experimental evidence that even when minimizing genetic and environmental differences, systematic individual differences in life-history measures and ultimately fitness can emerge.

Mapping the eco-evolutionary factors shaping the development of animals’ behavioural phenotypes remains a great challenge. Recent advances in ‘big behavioural data’ research—the high-resolution tracking of individuals and the harnessing of that data with powerful analytical tools—have vastly improved our ability to measure and model developing behavioural phenotypes. Applied to the study of behavioural ontogeny, the unfolding of whole behavioural repertoires can be mapped in unprecedented detail with relative ease. This overcomes long-standing experimental bottlenecks and heralds a surge of studies that more finely define and explore behavioural–experiential trajectories across development. In this review, we first provide a brief guide to state-of-the-art approaches that allow the collection and analysis of high-resolution behavioural data across development. We then outline how such approaches can be used to address key issues regarding the ecological and evolutionary factors shaping behavioural development: developmental feedbacks between behaviour and underlying states, early life effects and behavioural transitions, and information integration across development.

ABSTRACT Predation risk is a key driver of natural selection, influencing various aspects of prey behavior. While many studies focus on how predation risk affects average behavior at population level, less attention has been given to its potential impact on behavioral variation within prey populations. Here, we investigate the effect of perceived predation risk on among-individual behavioral variation in naturally clonal Amazon mollies. Juveniles were raised in two groups: one exposed to a predator during feeding (visual cues only) and the other one serving as a control group. We observed activity and feeding behavior (time spent feeding, visits to feeding spot) over a four-week period. (I) Individuals in the predator-exposed group were on average less active but there was no difference in average feeding behavior between the two groups, suggesting individuals strategically respond to threats based on behavior-specific cost-benefit trade-offs. (II) Among-individual behavioral variation was affected by perceived predation risk: in the absence of the predator, individuals developed pronounced differences in the time spent feeding while no such development was observed in the predator-exposed group. This result has the potential of affecting a wide range of fitness-relevant intraspecific interactions if lower among-individual feeding variation translate into reduced sizes differences. The presence of the predator initially reduced among-individual variation in activity and visits to the feeding spot, but these differences did not persist over time. Our findings highlight the importance of considering both population-level and individual-level responses to predation risk for a more comprehensive understanding of its ecological and evolutionary consequences.

Individuals continuously have to balance the error costs of alternative decisions. A wealth of research has studied how single individuals navigate this, showing that individuals develop response biases to avoid the more costly error. We, however, know little about the dynamics in groups facing asymmetrical error costs and when social influence amplifies either safe or risky behavior. Here, we investigate this by modeling the decision process and information flow with a drift-diffusion model extended to the social domain. In the model individuals first gather independent personal information; they then enter a social phase in which they can either decide early based on personal information, or wait for additional social information. We combined the model with an evolutionary algorithm to derive adaptive behavior. We find that under asymmetric costs, individuals in large cooperative groups do not develop response biases because such biases amplify at the collective level, triggering false information cascades. Selfish individuals, however, undermine the group's performance for their own benefit by developing higher response biases and waiting for more information. Our results have implications for our understanding of the social dynamics in groups facing asymmetrical errors costs, such as animal groups evading predation or police officers holding a suspect at gunpoint.

Behavioural individuality is a hallmark of animal life, with major consequences for fitness, ecology, and evolution. One of the most widely invoked explanations for this variation is that feedback loops between an animal's behaviour and its state (e.g. physiology, informational state, social rank, etc.) trigger and shape the development of individuality. Despite their often-cited importance, however, little is known about the ultimate causes of such feedbacks. Expanding on a previously employed model of adaptive behavioural development under uncertainty, we find that (i) behaviour-state feedbacks emerge as a direct consequence of adaptive behavioural development in particular selective environments and (ii) that the sign of these feedbacks, and thus the consequences for the development of behavioural individuality, can be directly predicted by the shape of the fitness function, with increasing fitness benefits giving rise to positive feedbacks and trait divergence and decreasing fitness benefits leading to negative feedbacks and trait convergence. Our findings provide a testable explanatory framework for the emergence of developmental feedbacks driving individuality and suggest that such feedbacks and their associated patterns of behavioural diversity are a direct consequence of adaptive behavioural development in particular selective environments.

Behavioral individuality is a ubiquitous phenomenon in animal populations, yet the origins and developmental trajectories of individuality, especially very early in life, are still a black box. Using a high-resolution tracking system, we mapped the behavioral trajectories of genetically identical fish ( Poecilia formosa ), separated immediately after birth into identical environments, over the first 10 weeks of their life at 3 s resolution. We find that (i) strong behavioral individuality is present at the very first day after birth, (ii) behavioral differences at day 1 of life predict behavior up to at least 10 weeks later, and (iii) patterns of individuality strengthen gradually over developmental time. Our results establish a null model for how behavioral individuality can develop in the absence of genetic and environmental variation and provide experimental evidence that later-in-life individuality can be strongly shaped by factors pre-dating birth like maternal provisioning, epigenetics and pre-birth developmental stochasticity.

Animals, including humans, differ in a wide range of physical and cognitive abilities ranging from measures of running speed and physical strength to learning ability and intelligence. We consider the evolution of ability when individuals interact pairwise over their contribution to a common good. In this interaction, the contribution of each is assumed to be the best given their own ability and the contribution of their partner. Since there is a tendency for individuals to partially compensate for a low contribution by their partner, low-ability individuals can do well. As a consequence, for benefit and cost structures for which individuals have a strong response to partner’s contribution, there can be selection for reduced ability. Furthermore, there can be disruptive selection on ability, leading to a bimodal distribution of ability under some modes of inheritance.

Decision makers in contexts as diverse as medical, judicial, and political decision making are known to differ substantially in response bias and accuracy, and these differences are a major factor undermining the reliability and fairness of the respective decision systems. Using theoretical modeling and empirical testing across five domains, we show that collective systems based on pooling decisions robustly overcome this important but as of now unresolved problem of experts' heterogeneity. In breast and skin cancer diagnostics and fingerprint analysis, we find that pooling the decisions of five experts reduces the variation in sensitivity among decision makers by 52%, 54%, and 41%, respectively. Similar reductions are achieved for specificity and response bias, and in other domains. Thus, although outcomes in individual decision systems are highly variable and at the mercy of individual decision makers, collective systems based on pooling decrease this variation, thereby promoting reliability, fairness, and possibly even trust.

Science requires replication. The development of many cloned or isogenic model organisms is a testament to this. But researchers are reluctant to use these traditional animal model systems for certain questions in evolution or ecology research, because of concerns over relevance or inbreeding. It has largely been overlooked that there are a substantial number of vertebrate species that reproduce clonally in nature. Here we highlight how use of these naturally evolved, phenotypically complex animals can push the boundaries of traditional experimental design and contribute to answering fundamental questions in the fields of ecology and evolution.