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The evolution of learning has long been hypothesized to be limited by fitness trade-offs such as delays in reproduction. We explored the relationship between host learning and reproduction in the cabbage white butterfly, Pieris rapae. The cabbage white female is innately biased to search for common green hosts but can learn to search for rare red h...
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... (control individu- als from Experiment 2) were held for 4 days following testing and all eggs laid on both red and green hosts were counted. Butterflies that had searched in the red host environment, relative to those in the green host environment, had signifi- cantly lower lifetime fecundity (Table 4 and Figure 5). Butter- flies that had searched for hosts in the complex nonhost environment, relative to those that had searched in the simple non-host environment, also had significantly lower lifetime fecundity (Table 4 and Figure 5). ...
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... that had searched in the red host environment, relative to those in the green host environment, had signifi- cantly lower lifetime fecundity (Table 4 and Figure 5). Butter- flies that had searched for hosts in the complex nonhost environment, relative to those that had searched in the simple non-host environment, also had significantly lower lifetime fecundity (Table 4 and Figure 5). ...
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... experience refers to the environment during host searching (red or green host nested within a simple or complex nonhost environment). Shown are least-square means from an ANOVA that also controls for full-sibling family and body size (see Table 4). ...
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... that such costs are specific to the environment in which the benefits of learning are experienced, these costs should, in theory, play less of a role than global costs in lim- iting the evolution of learning (see discussion in DeWitt et al. 1998). We found that butterflies with host searching experi- ence in the red host environment (relative to the green host environment) and the complex nonhost environment (rela- tive to the simple nonhost environment) had significantly lower lifetime fitness (Table 4 and Figure 5). For instance, butterflies with experience searching for red hosts had a 30% reduction in lifetime fitness relative to individuals with experience searching for green hosts ( Figure 5). ...
Citations
... new hosts or non-host environment). Females foraging in complex environments showed higher flight muscle development and, after gaining experience in this environment, increased offspring investment (higher egg size and lipid reserves) compared to females foraging in the control environment (Snell-Rood et al. 2011). The observed decrease in lifetime fecundity associated with an increase in cognition and learning capacities will lead to complex evolutionary life-history trade-offs in thermally costly environments (Dunlap et al. 2009;Snell-Rood et al. 2013). ...
Climate change alters many environmental parameters with strong consequences for ecological interactions, from species interactions to community dynamics. Temperature is crucial in determining ecosystem dynamics, especially for those involving ectothermic species such as plants or insects. Phenotypic plasticity, the capacity of one genotype to produce different phenotypes in response to environmental conditions, is a common mechanism by which individuals adapt to changing environments and is observed in multiple traits. The capacity of genotypes to adapt to novel temperature conditions plays a crucial role in structuring ecosystem dynamics and species persistence in adverse conditions. It is well recognised that temperature in natural ecosystems fluctuates over multiple time scales (e.g., hour, day, season, year). These fluctuations can follow predictable patterns or be unpredictable, with different consequences for phenotypic plasticity and ecosystem dynamics. Among trophic interactions, host–parasitoid interactions represent a special case because of the intimate symbiosis of the parasitoid larvae with their host. Understanding how and to what extent phenotypic plasticity structures species’ ecological niches is of utmost importance in the context of rapid climate change. With a particular focus on host–parasitoid interactions, this review discusses the literature on the role of phenotypic plasticity in fluctuating environments, highlighting the role of temporal dynamics. While we discuss literature on phenotypic plasticity at large, this review emphasises the fundamental effects of extreme temperatures in driving biochemical rates underlying phenotypic plasticity.
... Hence, in older (dominant) females the cost of maintaining a high reproductive output, even in the presence of competitors, might be traded-off against the maintenance of the energetically costly nervous system [13]. For example, experiments in the fruit fly and the cabbage white butterfly (Pieris rapae) have revealed a trade-off between learning performance and competitive ability [77] or female fecundity [78], respectively. In line with this explanation, when analysing long-term reproductive success in dominant babblers, we found that higher cognitive performance was associated with a lower number of fledglings produced per year. ...
Identifying the causes and fitness consequences of intraspecific variation in cognitive performance is fundamental to understand how cognition evolves. Selection may act on different cognitive traits separately or jointly as part of the general cognitive performance (GCP) of the individual. To date, few studies have examined simultaneously whether individual cognitive performance covaries across different cognitive tasks, the relative importance of individual and social attributes in determining cognitive variation, and its fitness consequences in the wild. Here, we tested 38 wild southern pied babblers (Turdoides bicolor) on a cognitive test battery targeting associative learning, reversal learning and inhibitory control. We found that a single factor explained 59.5% of the variation in individual cognitive performance across tasks, suggestive of a general cognitive factor. GCP varied by age and sex; declining with age in females but not males. Older females also tended to produce a higher average number of fledglings per year compared to younger females. Analysing over 10 years of breeding data, we found that individuals with lower general cognitive performance produced more fledglings per year. Collectively, our findings support the existence of a trade-off between cognitive performance and reproductive success in a wild bird.
... However, there are also costs associated with learning, potentially leading to trade-offs between learning and other traits, which may affect the net fitness benefits of learning. For example, faster learners were less competitive as larvae in Drosophila melanogaster (Mery & Kawecki, 2003), and more efficient learners were less fecund in cabbage white butterflies, Pieris rapae (Snell-Rood et al., 2011). Furthermore, performance on different learning tasks may be subject to trade-offs: individuals that make fast and strong initial associations may have more difficulty in reversal learning, which involves additional processes like proactive interference and inhibition. ...
Growing evidence suggests that individual variation in learning is ubiquitous, but why this is the case and what the consequences are is still a subject of much debate and research. One key set of explanations for variation in learning behaviour is that it relates to variation in animal personality traits. If personality traits affect how an individual interacts with its environment or processes information, this could directly affect performance in learning tasks. While this idea is generally well supported, there are inconsistent results on the relationships between specific personality traits and performance on different learning tasks, highlighting the need to measure multiple personality traits and to quantify different aspects of learning in the same individuals. We examined the relationship between three putative personality traits – aggression, latency to emerge from a shelter and time to contact a novel object – and learning speed in both initial and reversal olfactory learning in the house cricket, Acheta domesticus. Crickets were assayed for each personality trait, then tested for their speed to associate an odour with a water reward. Both aggression and latency to emerge were significantly repeatable, but only latency to emerge was related to learning speed, with individuals that took longer to emerge from the shelter requiring fewer trials to reach the learning criterion for both the initial and reversal learning experiments. We also identified sex differences in learning speed in the different experiments. Thus, our results provide some support for a relationship between personality and learning in an invertebrate.
... Second, empirical evidence suggests that the differential allocation of metabolic resources due to learning ultimately results in life-history (Burger, Kolss, Pont, & Kawecki, 2008;Snell-Rood, Davidowitz, & Papaj, 2011) and fitness trade-offs (Mery & Kawecki, 2003; see also Zwoinska, Lind, Cortazar-Chinarro, Ramsden, & Maklakov, 2016). Cognitive abilities, therefore, appear to evolve at some costs (Buchanan et al., 2013) i.e. the metabolic costs of building the neural substrates governing them (DeVoogd, 2004;Laughlin, de Ruyter van Steveninck, & Anderson, 1998;Lefebvre & Sol, 2008;Snell-Rood, Papaj, & Gronenberg, 2009) and the energetic and time costs related to the cognitive processes themselves, for example requiring sampling 85 Learned components of courtship of the environment (Mery & Kawecki, 2004). ...
Research into learning of courtship behavior remains largely confined to birdsong and vocal learning studies. Yet, visually communicated aspects of courtship displays are widespread and prominent, and also deserve consideration. Postural displays, choreographies, and construction of display arenas are all visual signal components mediated by motor activity of the displayer. The goal of this review is to present growing evidence for learning of courtship motor patterns other than song. We tackle two main challenges: we first highlight criteria that can be used to determine whether visual courtship components are learned, and if so, we then assess the type of learning involved. In line with the vocal learning literature, we suggest applying a distinction between usage learning and production learning of motor patterns: usage learning refers to a change in the context in which pre-existing display patterns are used, whereas production learning involves modification in trait structure, i.e. the acquisition of novel display patterns from a model. The effects of imitation, social feedback, and practice are described in detail, drawing on multiple examples from birdsong research. Our goals are to illustrate the learning processes which may affect motor development of courtship signals, to formulate testable predictions for each learning category and related mechanisms, and to suggest possible lines for future research. Although most of the evidence we review here is indirect and not yet conclusive about learning, recent technological advances now provide novel tools to quantify courtship motor patterns, and thus have the potential to produce more direct insights into whether, and how, courtship displays are learned.
... There are also operating costs associated with learning the unique features of many individuals, including the time, energy and resources required to collect, store and recall information. Long-term memory formation also reduces immunity, survival and fecundity [126,127]. ...
Animal groups are often organized hierarchically, with dominant individuals gaining priority access to resources and reproduction over subordinate individuals. Initial dominance hierarchy formation may be influenced by multiple interacting factors, including an animal's individual attributes, conventions and self-organizing social dynamics. After establishment, hierarchies are typically maintained over the long-term because individuals save time, energy and reduce the risk of injury by recognizing and abiding by established dominance relationships. A separate set of behaviours are used to maintain dominance relationships within groups, including behaviours that stabilize ranks (punishment, threats, behavioural asymmetry), as well as signals that provide information about dominance rank (individual identity signals, signals of dominance). In this review, we describe the behaviours used to establish and maintain dominance hierarchies across different taxa and types of societies. We also review opportunities for future research including: testing how self-organizing behavioural dynamics interact with other factors to mediate dominance hierarchy formation, measuring the long-term stability of social hierarchies and the factors that disrupt hierarchy stability, incorporating phenotypic plasticity into our understanding of the behavioural dynamics of hierarchies and considering how cognition coevolves with the behaviours used to establish and maintain hierarchies.
This article is part of the theme issue ‘The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies’.
... The presence of a lineage-specific male response to prior experience and a lineage-specific presence of assortative courtship suggest that H. m. malleti and H. m. rosina may experience different mating-related selective pressures. Maintaining the capacity to learn can be energetically costly and is often associated with fitness trade-offs, such as reduced fecundity (Kotrschal et al., 2013;Snell-Rood et al., 2011), reduced life span (Burger et al., 2008;Kotrschal et al., 2019) or extended development time (Kolss & Kawecki, 2008). Although H. m. malleti and H. m. rosina are conspecifics, they do not co-occur in nature (Brower, 1996;Rosser et al., 2012). ...
Many animals have the ability to learn, and some taxa have shown learned mate preference, which may be important for speciation. The butterfly Heliconius melpomene is a model system for several areas of research, including hybridization, mate selection and speciation, partially due to its widespread diversity of wing patterns. It remains unclear whether social experience shapes realized mating preferences in this species. Here we test whether previous experience with a female influences male mate preference for two H. melpomene subspecies, H. m. malleti and H. m. rosina. We conducted no-choice assays to determine whether male courtship (versus no courtship) and latency to court differed between naïve males and males with previous exposure to a sexually mature, virgin female. To test whether assortative courtship preference is learned in H. melpomene, males were either paired with a female who shared their phenotype or one who did not. Naïve H. m. malleti males courted assortatively, while naïve H. m. rosina males did not. When data were pooled across subspecies, experienced males reduced their courting relative to naïve males, suggesting that social experience with a female sans copulation may be perceived as a negative experience. This effect was likely driven by experienced H. m. malleti males, who reduced their courting relative to naïve males when analysed independently, while experienced H. m. rosina males did not. Our results suggest that social experience can influence male mating behaviour in H. melpomene and has the potential to contribute to the high rate of diversification observed in Heliconius butterflies.
... The shorter foraging careers of faster visual learners (Evans et al., 2017) was thought to have resulted from the energetic cost associated with enhanced cognitive performance, which can negatively impact other energetically demanding processes (Mery and Kawecki, 2003;Mery and Kawecki, 2004;Snell-Rood et al., 2011;Jaumann et al., 2013). Another study provides evidence of a "trade-off " in the opposite direction-increased foraging time lowered olfactory learning performance (reversal learning) among honey bees (Cabirol et al., 2018), further support for an inverse relationship between learning and foraging duration. ...
Individual animals allowed the opportunity to learn generally outperform those prevented from learning, yet, within a species the capacity for learning varies markedly. The evolutionary processes that maintain this variation in learning ability are not yet well understood. Several studies demonstrate links between fitness traits and visual learning, but the selection pressures operating on cognitive traits are likely influenced by multiple sensory modalities. In addition to vision, most animals will use a combination of hearing, olfaction (smell), gustation (taste), and touch to gain information about their environment. Some animals demonstrate individual preference for, or enhanced learning performance using certain senses in relation to particular aspects of their behaviour (e.g., foraging), whereas conspecific individuals may show different preferences. By assessing fitness traits in relation to different sensory modalities we will strengthen our understanding of factors driving observed variation in learning ability. We assessed the relationship between the olfactory learning ability of bumble bees (Bombus terrestris) and their foraging performance in their natural environment. We found that bees which failed to learn this odour-reward association had shorter foraging careers; foraging for fewer days and thus provisioning their colonies with fewer resources. This was not due to a reduced propensity to forage, but may have been due to a reduced ability to return to their colony. When comparing among only individuals that did learn, we found that the rate at which floral resources were collected was similar, regardless of how they performed in the olfactory learning task. Our results demonstrate that an ability to learn olfactory cues can have a positive impact of the foraging performance of B. terrestris in a natural environment, but echo findings of earlier studies on visual learning, which suggest that enhanced learning is not necessarily beneficial for bee foragers provisioning their colony.
... A third possible mechanism by which chronic stress may accelerate brain development is that young individuals process threat as an overall signal of lack of protection and support -that is, they receive cues that the environment requires maturity -and this triggers adaptive top-down processes that cause development to proceed more quickly. This was recently termed the 'developmental support hypothesis' (see reF. 93 ), and aligns with much evolutionary life-history research, including cross-species findings that parental investment is associated with slower maturation [93][94][95] . Understanding which, if any, of these mechanisms affect the pace of brain development is essential for determining when and how it might be possible to intervene. ...
Childhood socio-economic status (SES), a measure of the availability of material and social resources, is one of the strongest predictors of lifelong well-being. Here we review evidence that experiences associated with childhood SES affect not only the outcome but also the pace of brain development. We argue that higher childhood SES is associated with protracted structural brain development and a prolonged trajectory of functional network segregation, ultimately leading to more efficient cortical networks in adulthood. We hypothesize that greater exposure to chronic stress accelerates brain maturation, whereas greater access to novel positive experiences decelerates maturation. We discuss the impact of variation in the pace of brain development on plasticity and learning. We provide a generative theoretical framework to catalyse future basic science and translational research on environmental influences on brain development.
... The associated neural machinery and process of forming long-term memories are metabolically costly (Laughlin et al. 1998;Mery and Kawecki 2005), and large brains result in exponential increases in developmental time (Workman et al. 2013). Thus, the evolution of learning results in tradeoffs in juvenile competitive ability (Mery and Kawecki 2003) and adult reproduction, often delaying reproduction and resulting in greater investment in fewer offspring (Barrickman et al. 2008;Snell-Rood et al. 2011;Kotrschal et al. 2013). In many cases, there are even direct tissue tradeoffs between plasticity machinery (such as brain size) and other costly tissues, such as gut or flight muscle (Isler and van Schaik 2006;Liao et al. 2016). ...
... Therefore, investment in learning and the maintenance of learning skills can result in trade-offs with investments in other biological functions. Previous studies have confirmed this expectation and showed that in some species, the ability to learn is associated with delayed reproduction , 2004Snell-Rood et al. 2011). This phenomenon occurs because resources that might be invested in reproductive tissue are redirected to development and maintenance of energetically expensive neural tissue, which is required for learning and memory (Laughlin et al. 1998). ...
... Studies that have evaluated trade-offs between learning ability and other life functions are not limited to fruit flies. Negative correlations between learning ability and trade-offs were found in butterflies (Pieris rapae ) (Snell-Rood et al. 2011), antlion (Myrmeleon bore ) larvae ) and predatory mites (Phytoseiidae) (Christiansen et al. 2016). ...
... All previous studies that focused on trade-offs between learning skills and the reproductive potential of individuals focused on solitary species (e.g., Mery and Kawecki 2004;Mery and Kawecki 2005;Snell-Rood et al. 2011). However, the honeybee is a eusocial species, where individuals live together and the whole society is involved in the raising of the queen's offspring. ...
Learning ability, which allows individuals to adjust their behaviour to changing environmental conditions, has a considerable positive impact on individual fitness. However, in addition to benefits, learning also incurs a cost, which means that investment in learning and maintaining learned skills can lead to trade-offs impacting other biological functions. Here, we tested whether a trade-off exists between learning skills and reproductive potential in honeybee workers. For this purpose, we compared learning ability between two groups of workers that differed in reproductive potential—normal and rebel workers. The results showed that workers with high reproductive potential (rebels), measured according to the number of ovarioles in the ovary, learned faster than normal workers with low reproductive potential. Moreover, by performing separate regression analyses within the rebel and non-rebel worker groups, we found that the reproductive potential of workers was positively correlated with their learning ability. The results show that in honeybees, there is no trade-off in resource allocation between two costly biological functions, learning and reproduction.
