Early life experiences can have latent effects, which could manifest at a later stage of life history. Though the carryover effects of predation on the behaviour of prey are well-known, the integrative effects of predation on the growth, behaviour, and morphology of prey are less known. Hence, we used early (Gosner stages 10–14) and late (stages 15–19) embryonic stages of Euphlyctis cyanophlyctis to determine the carryover effects of predation risk on larval growth, behaviour, morphology, and metamorphic traits. Early and late embryonic stages were exposed to cues of predation risk to assess their antipredator responses later during larval life and at metamorphosis. The results show that embryonic exposure to cues of predation risk elicits antipredator behavioural responses towards kairomones of the dragonfly nymphs at the larval stage. Late embryonic stages exposed to cues of predation risk grew faster as larvae and displayed stronger antipredator responses than those exposed during early embryonic stages. Further, early embryonic stages facing cues of predation risk developed narrow bodies and longer tails as tadpoles. However, late embryonic stages facing cues of predation risk accrued greater body mass had narrow tails with greater tailfin heights and deeper tail muscles as tadpoles. The carryover effects of embryonic exposure to cues of predation risk were also apparent at metamorphosis. Embryos exposed during early stages metamorphosed earlier with larger body size. In contrast, embryos exposed to cues of predation risk at later stages metamorphosed earlier with larger length. Thus, the results of our study suggest that embryonic exposure to cues of larval predation induces latent behavioural and developmental carryover effects similar to those displayed by tadpoles facing predation risk.
Recognizing early life dangers may help animals to respond to such dangers later in their life. In this study, for the first time, we show the integrative effects of embryonic exposure to cues of predation risk on growth, behaviour, morphology and life history traits of larval life of the skipper frogs. In the skipper frogs, embryonic exposure to cues of predation risk induces behavioural and developmental effects similar to those shown by tadpoles facing predation risk.
Over their lifetime, individuals may use different behavioural strategies to maximize their fitness. Some behavioural traits may be consistent among individuals over time (i.e., ‘personality’ traits) resulting in an individual behavioural phenotype with different associated costs and benefits. Understanding how behavioural traits are linked to lifetime fitness requires tracking individuals over their lifetime. Here, we leverage a long-term study on a multi-year living species (maximum lifespan ~ 10 years) to examine how docility (an individual’s reaction to trapping and handling) may contribute to how males are able to maximize their lifetime fitness. Cape ground squirrels are burrowing mammals that live in social groups, and although males lack physical aggression and territoriality, they vary in docility. Males face high predation risk and high reproductive competition and employ either of two reproductive tactics (‘natal’ or ‘band’) which are not associated with different docility personalities. We found that although more docile individuals sired more offspring on an annual basis, docility did not affect an individual’s long-term (lifetime) reproductive output. Survival was not associated with docility or body condition, but annual survival was influenced by rainfall. Our findings suggest that although docility may represent a behavioural strategy to maximize fitness by possibly playing a role in female-male associations or female mate-choice, variations in docility within our study population is likely maintained by other environmental drivers. However, individual variations in behaviours may still contribute as part of the ‘tool kit’ individuals use to maximize their lifetime fitness.
Multilevel societies (MLS), which are characterized by two or more levels of social organization, are among the most complex primate social systems. MLS have only been recorded in a limited number of primates, including humans. The aim of this study was to investigate whether proboscis monkeys (Nasalis larvatus) form MLS in Sabah, Malaysia, and to genetically characterize their dispersal patterns. Association data were obtained through direct observation (35 months) and kinship data through genetic analysis, based on feces collected from ~ 200 individuals. The results strongly suggest that proboscis monkeys exhibit a form of MLS, with several core reproductive units and a bachelor group woven together into a higher-level band. Genetic analysis revealed that the females migrated randomly over short and long distances; however, the males tended to migrate relatively shorter distances than females. Furthermore, male-male dyads showed a slightly higher average relatedness than female-female dyads. Combined with the results of direct observations, we conclude that proboscis monkeys form MLS with at least two layers and a patrilineal basis. Since patrilineal MLS have been identified as an important step in the evolution of human societies, their convergent appearance in proboscis monkeys may help us understand the drivers of human social evolution.
The aim of this study was to determine the social organization of proboscis monkeys by direct observation and genetic analysis. The results revealed that their social system exhibited a form of multilevel society with a possible patrilineal basis. Since humans exhibit a similar constellation of social features, proboscis monkeys may offer insightful clues about human social evolution.
Abstract: The role of visual search during bee foraging is relatively understudied compared to the choices made by bees. As bees learn about rewards, we predicted that visual search would be modified to prioritise rewarding flowers. To test this, we ran an experiment testing how bee search differs in the initial and later part of training as they learn about flowers with either higher- or lower-quality rewards. We then ran an experiment to see how this prior training with reward influences their search on a subsequent task with different flowers. We used the time spent inspecting flowers as a measure of attention and found that learning increased attention to rewards and away from unrewarding flowers. Higher quality rewards led to decreased attention to non-flower regions, but lower quality rewards did not. Prior experience of lower rewards also led to more attention to higher rewards compared to unrewarding flowers and non-flower regions. Our results suggest that flowers would elicit differences in bee search behaviour depending on the sugar content of their nectar. They also demonstrate the utility of studying visual search and have important implications for understanding the pollination ecology of flowers with different qualities of reward.
Significance statement: Studies investigating how foraging bees learn about reward typically focus on the choices made by the bees. How bees deploy attention and visual search during foraging is less well studied. We analysed flight videos to characterise visual search as bees learn which flowers are rewarding. We found that learning increases the focus of bees on flower regions. We also found that the quality of the reward a flower offers influences how much bees search in non-flower areas. This means that a flower with lower reward attracts less focussed foraging compared to one with a higher reward. Since flowers do differ in floral reward, this has important implications for how focussed pollinators will be on different flowers. Our approach of looking at search behaviour and attention thus advances our understanding of the cognitive ecology of pollination.
Supplementary information: The online version contains supplementary material available at 10.1007/s00265-024-03432-z.
Favoring males’ specific sexual signals, female preferences play a major role in frogs’ evolutionary process by selecting traits linked to those signals. However, the factors constraining and determining those preferences are scarcely explored in an evolutionary background. Here, through a phylogenetic comparative approach we check whether anuran species phylogenetic proximity and calling site predicts female preferences for dominant frequency and whether those preferences influence species sexual size dimorphism. Our hypotheses are as follows: 1) closer species have similar females’ preferences related to the dominant frequency of the partners’ calls; 2) the calling site influences sound propagation and consequently the preference of females for the dominant frequency of the males’ calls; and 3) the preference for calls with low dominant frequency influences the size of the males and consequent reduction of the biSased dimorphism for females. We did not find support for our hypotheses, neither for the influence of phylogenetic proximity nor for calling site determining these preferences. Moreover, female preferences did not impact on species sexual size dimorphism. Besides shedding light into our hypotheses, this study represents a considerable advance on evolutionary studies of female preferences in anura, which still lacks broad species comparative approaches. Furthermore, we suggest future studies to expand knowledge regarding frogs’ female preferences.
This study advances our comprehension of female preferences in frogs by investigating the factors that shape these preferences and their implications for species sexual size dimorphism. Utilizing phylogenetic comparative methods, an approach rarely used in the context of anuran female preferences, this study represents a significant step in applying broad comparative approaches in this field. Highlighting the complex nature of mate choice and its relationship to morphology, soundscape, and phylogeny, we present important insights into evolutionary hypotheses related to female preferences. Lastly, we provide advice on how future studies could further explore this topic in a broader comparative framework while also discussing the limitations of available data on anuran mating preferences.
In uncertain environments, animals often face the challenge of deciding whether to stay with their current foraging option or leave to pursue the next opportunity. The voluntary decision to persist at a location or with one option is a critical cognitive ability in animal temporal decision-making. Little is known about whether foraging insects form temporal expectations of reward and how these expectations affect their learning and rapid, short-term foraging decisions. Here, we trained bumblebees on a simple colour discrimination task whereby they entered different opaque tunnels surrounded by coloured discs (artificial flowers) and received reinforcement (appetitive sugar water or aversive quinine solution depending on flower colour). One group received reinforcement immediately and the other after a variable delay (0–3 s). We then recorded how long bees were willing to wait/persist when reinforcement was delayed indefinitely. Bumblebees trained with delays voluntarily stayed in tunnels longer than bees trained without delays. Delay-trained bees also waited/persisted longer after choosing the reward-associated flower compared to the punishment-associated flower, suggesting stimulus-specific temporal associations. Strikingly, while training with delayed reinforcement did not affect colour discrimination, it appeared to facilitate the generalisation of temporal associations to ambiguous stimuli in bumblebees. Our findings suggest that bumblebees can be trained to form temporal expectations, and that these expectations can be incorporated into their decision-making processes, highlighting bumblebees’ cognitive flexibility in temporal information usage.
The willingness to voluntarily wait or persist for potential reward is a critical aspect of decision-making during foraging. Investigating the willingness to persist across various species can shed light on the evolutionary development of temporal decision-making and related processes. This study revealed that bumblebees trained with delays to reinforcement from individual flowers were able to form temporal expectations, which, in turn, generalised to ambiguous stimuli. These findings contribute to our understanding of temporal cognition in an insect and the potential effects of delayed rewards on foraging behaviour.
A well-established field of research in vertebrates focuses on the variability of cognitive abilities within species. From mammals to fish, numerous studies have revealed remarkable differences in the cognitive phenotype among individuals, particularly in terms of sex or personality. However, many aspects of the mechanisms, genetics, and selective pressures that underlie individual cognitive variation remain unclear. Surprisingly, intraspecific variability in cognition has received much less attention in invertebrates, despite the increasing evidence of remarkable cognitive abilities in this group and the insights that could be gained from examining simultaneously two distinct taxa, namely vertebrates and invertebrates. In this review, we provide evidence that certain invertebrate species exhibit all the key features of cognitive variation observed in vertebrates, including differences related to sex and personality. In many cases, invertebrate studies have provided insights into the genetic basis, evolvability and response to selection of cognitive variability. Moreover, we highlight evidence for caste differences in eusocial insects, which are linked to task specialisation within the colony. This makes insect eusociality a valuable system for understanding how selection influences cognitive variation. We propose that cognitive variation in invertebrates may be more widespread than currently thought, and that selection may operate in a similar manner on two distantly related cognitive systems (vertebrates and invertebrates). Finally, we suggest that invertebrates hold the potential to serve both as alternative and complementary models to vertebrates, contributing to a deeper understanding of cognitive evolution.
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