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BACKGROUND: Evolutionary medicine builds on evolutionary biology and explains why natural selection has left us vulnerable to disease. Unfortunately, several misunderstandings exist in the medical literature about the levels and mechanisms of evolution. Reasons for these problems start from the lack of teaching evolutionary biology in medical schools. A common mistake is to assume that "traits must benefit the species, as otherwise the species would have gone extinct in the past" confusing evolutionary history (phylogeny) with evolutionary function (fitness). SUMMARY: Here we summarise some basic aspects of evolutionary medicine by pointing out: (1) Evolution has no aim. (2) For adaptive evolution to occur, a trait does not have to be beneficial to its carrier throughout its entire life. (3) Not every single individual carrying an adaptive trait needs to have higher than average fitness. (4) Traits do not evolve for the benefit of the species. Using examples from the field of neuroimmunomodulation like sickness behaviour (nervous system), testosterone (hormones), and cytokines (immunity), we show how misconceptions arise from not differentiating between the explanatory categories of phylogeny (evolutionary history) and evolutionary function (fitness). KEY MESSAGES: Evolution has no aim but is an automatism that does not function for the benefit of the species. In evolution, successful individuals are those that maximise the transmission of their genes, and health and survival are just strategies to have the opportunity to do so. Thus, a trait enabling survival of the individual until reproductive age will spread even if at later age the same trait leads to disease and death. Natural and sexual selection do not select for traits that benefit the health or happiness of the individual, but for traits that increase inclusive fitness even if this increases human suffering. In contrast, our humane aim is to increase individual well-being. Evolutionary medicine can help us achieve this aim against evolutionary constraints.
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Evolución Biológica , Neuroinmunomodulación , Humanos , Neuroinmunomodulación/fisiología , Animales , Filogenia , Selección GenéticaRESUMEN
Cognition is shaped by evolution and is predicted to increase fitness. However, the link between cognition and fitness in free-living animals is unresolved. We studied the correlates of cognition and survival in a free-living rodent inhabiting an arid environment. We tested 143 striped mice (Rhabdomys pumilio) using a battery of cognitive tests, including: (i) an attention task, (ii) two problem-solving tasks, (iii) a learning and reversal learning task, and (iv) an inhibitory control task. We related cognitive performance with days of survival. Better problem-solving and inhibitory control performance were significant correlates of survival. Surviving males showed greater reversal learning which may be related to sex-specific behavioural and life-history characteristics. Specific cognitive traits and not a composite measure of general intelligence underpins fitness in this free-living rodent population, enhancing our understanding of the evolution of cognition in non-human animals.
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Cognición , Murinae , Animales , Femenino , Masculino , Solución de Problemas , Aprendizaje InversoRESUMEN
We must differentiate between stressful and harsh environments to understand animals' resilience to global change. Harshness is not stress. Stressful environments activate the physiological stress response to increase energy availability, while harsh environments inhibit the physiological stress response to save energy.
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Ambiente , Estrés Fisiológico , AnimalesRESUMEN
Innovative problem-solving ability is a predictor of whether animals can successfully cope with environmental changes. These environmental changes can test the limits of animals, for example when energy availability decreases seasonally and, hence, problem-solving performance decreases because less energy is available for cognitive processes. Here, we investigated: (1) how problem-solving performance changed between seasons that differed significantly in food availability; (2) whether these changes were related to environmentally induced physiological changes in blood glucose and ketone levels, indicators of energy availability; and (3) whether individual variation in problem-solving was related to sex differences. We studied 99 free-ranging African striped mice, Rhabdomys pumilio, in the Succulent Karoo, South Africa, 55 during the hot dry summer with low food availability and 44 during the cold wet winter with higher food availability. We measured their problem-solving abilities using a food extraction task and found no seasonal differences in problem-solving success. However, mice solved the problem faster in summer versus winter. In summer, food availability was reduced and blood ketones increased but there was no seasonal difference in blood glucose levels. There were no correlation between problem-solving performance and blood glucose or ketone levels. Overall, more males solved the task than females. It appears that in striped mice cognitive functions can be maintained under harsh environmental conditions.
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Murinae , Solución de Problemas , Animales , Cognición/fisiología , Femenino , Alimentos , Masculino , Ratones , Murinae/fisiología , Estaciones del AñoRESUMEN
Most scientists agree that we have to restrict climate change, but there is much frustration that we are failing. The Corona Crisis exemplifies how human behavior is constrained by its evolution, cognition, and resource availability, explaining why we do not act to avoid climate change for the benefit of future generations.
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Cambio Climático , HumanosRESUMEN
In changing environments, animals face unexpected problems to solve. Not all individuals in a population are equally able to solve new problems. It still remains unclear what factors (e.g. age and body condition) influence the propensity of problem solving. We investigated variation in problem-solving performance among males following alternative reproductive tactics (ARTs). We studied a free-ranging population of the African striped mouse (Rhabdomys pumilio). Adult male striped mice can employ 3 ARTs: (1) dominant group-living breeders, (2) philopatric living in their natal group, and (3) solitary-living roamers. ARTs in male striped mice reflect differences in competitiveness, sociality and physiology which could influence their problem-solving performance. We tested a total of 48 males in 2 years with two tasks: a string-pulling task to reach food and a door-opening task to reach the nest. Since male striped mice differ in personality traits independent of ARTs, we also measured activity, boldness and exploration. In addition, we assessed the association of body condition and age with problem solving. Problem solving was related the interaction of age and ARTs. The younger philopatrics had better performance in a food-extraction task whereas the older breeders were faster at solving the door-opening task. Individual differences in traits related to personality were significant correlates of problem-solving performance: pro-active mice (i.e. more active and explorative and bolder) performed better in both tasks. Finally, problem-solving performance was not consistent between the two tasks. Our study provides evidence of correlates of ARTs, age and personality on problem-solving abilities.
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Reproducción , Conducta Sexual Animal , Animales , Masculino , Ratones , Murinae , Solución de Problemas , Conducta SocialRESUMEN
Telomere shortening has been used as an indicator of aging and is believed to accelerate under harsh environmental conditions. This can be attributed to the fact that telomere shortening has often been regarded as non-reversible and negatively impacting fitness. However, studies of laboratory mice indicate that they may be able to repair telomere loss to recover from environmental harshness, as indicated by recent studies in hibernating rodents. We studied seasonal variation in telomere dynamics in African striped mice (Rhabdomys pumilio) living in a highly seasonal environment. In our annual species, individuals born in the moist spring (high food availability) need to survive the harsh dry summer (low food availability) to be able to reproduce in the following spring. We studied the effect of the harsh dry vs. the benign moist season on telomere dynamics. We also tested if telomere length or the rate of change in telomere length over the dry season predicted the probablity of dissapearance from the population at the same time. Male, but not female, stripped mice showed age-related telomere erosion. Telomeres were longer at the beginning of the dry season compared to the rest of the year. Telomeres increased significantly in length during the moist season. Neither telomere length at the onset of the dry season nor telomere loss over the dry season predicted whether or not individuals disappeared. In conclusion, our data suggest that seasonal attrition and restoring of telomeres also occurs in non-hibernating wild rodents living in hot food restricted environments.
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Murinae , Telómero , Envejecimiento , Animales , Alimentos , Humanos , Masculino , Ratones , Murinae/genética , Estaciones del Año , Acortamiento del TelómeroRESUMEN
Individuals that are capable of accumulating appropriate fat stores are assumed to have selective advantages when food becomes scarce. Similarly to species from temperate zones, some species inhabiting arid areas accumulate fat stores prior to periods of food limitation. Yet, we have little knowledge concerning seasonal variation in body composition and the relationship between fat store size and disappearance risk in species from arid habitats. Using the water dilution method, we examined the body composition of African striped mice (Rhabdomys pumilio) living in a seasonal habitat with a long food-restricted dry season. We tested for seasonal changes in body composition (N=159 measurements of 113 individuals) and whether dry season survival was related to fat mass (N=66 individuals). Fat stores were similar in size at the onset and the end of the dry season, but surprisingly smaller at the onset of the moist breeding season. Fat stores showed a negative relationship with food availability. Individual variation in fat stores was not associated with disappearance risk, but there was a positive association of disappearance risk with body mass. Increased disappearance risk of heavy individuals suggests elevated dispersal rates in competitive individuals. This study suggests that non-breeding philopatric striped mice do not accumulate large fat stores prior to the food-limited dry season but that they might mobilize fat stores at the onset of the breeding season to satisfy the energetic demands of reproduction and/or to decrease costs associated with larger fat stores, such as increased predation risk.
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Composición Corporal , Conducta Alimentaria , Longevidad , Murinae/fisiología , Reproducción , Adiposidad , Animales , Femenino , Masculino , Estado de Hidratación del Organismo , Estaciones del Año , Sudáfrica , AguaRESUMEN
According to the cort-fitness hypothesis, glucocorticoid levels correlate negatively with fitness. However, field studies found mixed support for this hypothesis, potentially because the association between glucocorticoids and fitness might depend on prevailing environmental conditions. Based on the long-term monitoring of a natural rodent population, we tested whether individuals with elevated corticosterone levels were more likely to disappear, accounting for individual condition and among-year variation in food availability, population density and predation pressure. We used basal corticosterone levels measured at the onset of the pre-breeding season in 331 African striped mice from six generations. While basal corticosterone levels were highly repeatable within individuals, between-individual variation was large. Survival analysis revealed that disappearance risk over the pre-breeding season increased with elevated basal corticosterone levels for light but not for heavy individuals. High levels of corticosterone may be more deleterious to smaller individuals (i.e. through allostatic overload), eventually increasing their mortality risk, and disappearance would represent actual death. An alternative non-exclusive explanation could be that high levels of corticosterone selectively trigger dispersal in light individuals, and disappearance would rather reflect their departure from the population. Although environmental conditions varied considerably among generations, none of the interactions between corticosterone and environmental variables were significant. Disappearance probability was positively correlated with both predation pressure and with food availability, a factor favoring dispersal. In sum, elevated basal corticosterone levels increased disappearance in light striped mice, either directly via reduced survival prospects and/or indirectly via dispersal.
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Distribución Animal/fisiología , Peso Corporal/fisiología , Corticosterona/sangre , Longevidad/fisiología , Roedores/fisiología , Animales , Ambiente , Femenino , Cadena Alimentaria , Abastecimiento de Alimentos , Glucocorticoides/sangre , Masculino , Ratones , Monitoreo Fisiológico/métodos , Monitoreo Fisiológico/veterinaria , Aptitud Física/fisiología , Reproducción/fisiología , Roedores/sangre , Estaciones del Año , Sudáfrica , Análisis de SupervivenciaRESUMEN
In many species, males follow alternative reproductive tactics (ARTs), where one tactic (called bourgeois) has much higher reproductive success than alternative tactics followed by males with lower competitive ability. The extent to which ARTs differ in energetic costs is unknown, but it is important to understand the fitness payoffs of ARTs. We studied male African striped mice (Rhabdomys pumilio) which follow one of three ARTs: heavy bourgeois males defend harems of females and have 10 times higher reproductive success than smaller roamers, which have ten times higher reproductive success than philopatric males, which remain in their natal group and are the smallest males. Bourgeois and philopatric males live in social groups that defend one territory, while roamers are solitary and roam over larger areas. We predicted that roamers will face higher energetic costs compared to group-living males because they do not gain thermoregulatory benefits of huddling in groups and might travel larger distances as they have larger home ranges. We measured daily energy expenditure (DEE) of 30 males, resting metabolic rate (RMR) of 79 males, travel distances and daily ranges of 31 males and changes in body mass of 51 males. Roamers had higher DEE and higher RMR than both types of group-living males. Philopatric males had shorter travel distances and smaller daily ranges than both roamers and bourgeois males, which did not differ from each other. This indicates that the higher DEE of roamers compared to bourgeois males cannot be explained by larger travel distances. Philopatrics gained body mass faster than bourgeois males and roamers, thereby increasing their competitive ability and thus the probability of later switching to a tactic of higher reproductive success. Our results suggest that roamers suffer energetic costs that might reduce their ability of gaining body mass and thus the likelihood of switching to the bourgeois tactic, indicating evolutionary trade-offs between investing energy into roaming versus gaining body mass.
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Metabolismo Energético/fisiología , Reproducción/fisiología , Conducta Sexual Animal/fisiología , Conducta Social , Animales , Peso Corporal/fisiología , Masculino , MurinaeRESUMEN
Population dynamics are the result of an interplay between extrinsic and intrinsic environmental drivers. Predicting the effects of environmental change on wildlife populations therefore requires a thorough understanding of the mechanisms through which different environmental drivers interact to generate changes in population size and structure. In this study, we disentangled the roles of temperature, food availability and population density in shaping short- and long-term population dynamics of the African striped mouse, a small rodent inhabiting a semidesert with high intra- and interannual variation in environmental conditions. We parameterized a female-only stage-structured matrix population model with vital rates depending on temperature, food availability and population density, using monthly mark-recapture data from 1609 mice trapped over 9 years (2005-2014). We then applied perturbation analyses to determine relative strengths and demographic pathways of these drivers in affecting population dynamics. Furthermore, we used stochastic population projections to gain insights into how three different climate change scenarios might affect size, structure and persistence of this population. We identified food availability, acting through reproduction, as the main driver of changes in both short- and long-term population dynamics. This mechanism was mediated by strong density feedbacks, which stabilized the population after high peaks and allowed it to recover from detrimental crashes. Density dependence thus buffered the population against environmental change, and even adverse climate change scenarios were predicted to have little effect on population persistence (extinction risk over 100 years <5%) despite leading to overall lower abundances. Explicitly linking environment-demography relationships to population dynamics allowed us to accurately capture past population dynamics. It further enabled establishing the roles and relative importances of extrinsic and intrinsic environmental drivers, and we conclude that doing this is essential when investigating impacts of climate change on wildlife populations.
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Cambio Climático , Roedores , Animales , Demografía , Femenino , Ratones , Densidad de Población , Dinámica PoblacionalRESUMEN
Animals that spend more energy than they obtain risk entering allostatic overload, reducing survival and fitness. They are predicted to adjust their daily energy expenditure (DEE) during periods of food scarcity. Adjustments of DEE to changes in food availability have been well-studied in species in temperate zones during winter, but less so in species enduring seasonal droughts. Likely mechanisms regulating DEE involve adjustments of activity and maintenance metabolism. Species that experience seasonal droughts and changes in food availability, like the African striped mouse (Rhabdomys pumilio), are appropriate model organisms to study the regulation of seasonal changes of DEE. We quantified DEE using the 'doubly labelled water' method, measured resting metabolic rate (RMR), and concomitantly determined activity levels using all-day focal observations of 69 free-living striped mice in the cold moist season with high food availability and the hot dry season with low food availability. Striped mice decreased their DEE in the food scarce dry season using multiple mechanisms, especially reductions in RMR, and reduced overall physical activity. This was further facilitated passively by reduced thermoregulatory costs. Our study demonstrates that animals reduce DEE via active and passive mechanisms in food-restricted environments, and highlights that several environmental factors should be considered simultaneously when aiming to understand how animals cope with harsh environments.
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Metabolismo Energético , Estaciones del Año , Animales , Sequías , Femenino , Alimentos , Locomoción , Masculino , Ratones , Lluvia , TemperaturaRESUMEN
Family groups with helpers occur in several species of fish, birds and mammals. In such cooperatively breeding species all group members help with raising the offspring, i.e. parents and offspring from previous litters. While the ecological reasons and ultimate consequences of allo-parental care have been studied in detail, we know little about its physiological regulation. We propose three alternative hypotheses for the endocrine regulation of allo-parental care. 1. The neoteny-helper hypothesis predicts that helpers that did not undergo adolescence yet show helping behavior without any endocrine mechanisms activating it, as helping is the default response towards infant stimuli. The endocrine changes during adolescence would then deactivate helping behavior. 2. The parent-helper hypothesis predicts that helpers undergo the same endocrine changes as parents (increased prolactin and corticosterone levels; decreased testosterone in males but increased estrogen in females). We predict that this hypothesis is especially important in post-adolescent helpers. 3. The helper-specific hypothesis predicts that there are specific endocrine mechanisms that only exist in helpers but not in breeders. We review evidence for these three hypotheses in 23 species of fish, birds, and mammals. We found no evidence for the helper-specific hypothesis but for both other hypotheses. As predicted, this depended on whether helpers were pre- or post-adolescent, but information on whether or not helpers underwent adolescence was often missing. Thus, future studies should investigate whether or not helpers have reached sexual maturity, differentiate between pre- and post-adolescent helpers, and study behavioral changes in helping behavior during adolescence. We conclude that the neurobiological circuits in the brain necessary for allo-parental care might often be the default stage in helpers from cooperative breeding species, which might be deactivated by specific endocrine mechanisms during adolescence, and then would need reactivation for allo-parental and parental care.
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Conducta Animal/fisiología , Hormonas/metabolismo , Conducta Materna/fisiología , Modelos Biológicos , Conducta Paterna/fisiología , Animales , Conducta de Ayuda , Maduración Sexual/fisiologíaRESUMEN
Mallarino et al. introduce the African striped mouse, which is being used in a number of fields of research, including animal behavior, evolutionary developmental biology, and chronobiology.