Longevity is associated with relative brain size in birds

Brain size of vertebrates has long been recognized to evolve in close association with basic life‐history traits, including lifespan. According to the cognitive buffer hypothesis, large brains facilitate the construction of behavioral responses against novel socioecological challenges through general cognitive processes, which should reduce mortality and increase lifespan. While the occurrence of brain size–lifespan correlation has been well documented in mammals, much less evidence exists for a robust link between brain size and longevity in birds. The aim of this study was to use phylogenetically controlled comparative approach to test for the relationship between brain size and longevity among 384 avian species from 23 orders. We used maximum lifespan and maximum reproductive lifespan as the measures of longevity and accounted for a set of possible confounding effects, such as allometry, sampling effort, geographic patterns, and life‐history components (clutch size, incubation length, and mode of development). We found that both measures of longevity positively correlated with relative (residual) brain size. We also showed that major diversification of brain size preceded diversification of longevity in avian evolution. In contrast to previous findings, the effect of brain size on longevity was consistent across lineages with different development patterns, although the relatively low strength of this correlation could likely be attributed to the ubiquity of allomaternal care associated with the altricial mode of development. Our study indicates that the positive relationship between brain size and longevity in birds may be more general than previously thought.     

Light enough to travel or wise enough to stay? Brain size evolution and migratory behavior in birds

Brain size relative to body size is smaller in migratory than in nonmigratory birds. Two mutually nonexclusive hypotheses had been proposed to explain this association. On the one hand, the “energetic trade‐off hypothesis” claims that migratory species were selected to have smaller brains because of the interplay between neural tissue volume and migratory flight. On the other hand, the “behavioral flexibility hypothesis” argues that resident species are selected to have higher cognitive capacities, and therefore larger brains, to enable survival in harsh winters, or to deal with environmental seasonality. Here, I test the validity and setting of these two hypotheses using 1466 globally distributed bird species. First, I show that the negative association between migration distance and relative brain size is very robust across species and phylogeny. Second, I provide strong support for the energetic trade‐off hypothesis, by showing the validity of the trade‐off among long‐distance migratory species alone. Third, using resident and short‐distance migratory species, I demonstrate that environmental harshness is associated with enlarged relative brain size, therefore arguably better cognition. My study provides the strongest comparative support to date for both the energetic trade‐off and the behavioral flexibility hypotheses, and highlights that both mechanisms contribute to brain size evolution, but on different ends of the migratory spectrum.     

Effects of seasonality on brain size evolution: evidence from strepsirrhine primates

Seasonal changes in energy supply impose energetic constraints that affect many physiological and behavioral characteristics of organisms. As brains are costly, we predict brain size to be relatively small in species that experience a higher degree of seasonality (expensive brain framework). Alternatively, it has been argued that larger brains give animals the behavioral flexibility to buffer the effects of habitat seasonality (cognitive buffer hypothesis). Here, we test these two hypotheses in a comparative study on strepsirrhine primates (African lorises and Malagasy lemurs) that experience widely varying degrees of seasonality. We found that experienced seasonality is negatively correlated with relative brain size in both groups, controlling for the effect of phylogenetic relationships and possible confounding variables such as the extent of folivory. However, relatively larger-brained lemur species tend to experience less variation in their dietary intake than indicated by the seasonality of their habitat. In conclusion, we found clear support for the hypothesis that seasonality restricts brain size in strepsirrhines as predicted by the expensive brain framework and weak support for the cognitive buffer hypothesis in lemurs.     

Big-brained birds survive better in nature

Big brains are hypothesized to enhance survival of animals by facilitating flexible cognitive responses that buffer individuals against environmental stresses. Although this theory receives partial support from the finding that brain size limits the capacity of animals to behaviourally respond to environmental challenges, the hypothesis that large brains are associated with reduced mortality has never been empirically tested. Using extensive information on avian adult mortality from natural populations, we show here that species with larger brains, relative to their body size, experience lower mortality than species with smaller brains, supporting the general importance of the cognitive buffer hypothesis in the evolution of large brains.     

Large‐brained mammals live longer

Many mammals have brains substantially larger than expected for their body size, but the reasons for this remain ambiguous. Enlarged brains are metabolically expensive and require elongated developmental periods, and so natural selection should have favoured their evolution only if they provide counterbalancing advantages. One possible advantage is facilitating the construction of behavioural responses to unusual, novel or complex socio‐ecological challenges. This buffer effect should increase survival rates and favour a longer reproductive life, thereby compensating for the costs of delayed reproduction. Here, using a global database of 493 species, we provide evidence showing that mammals with enlarged brains (relative to their body size) live longer and have a longer reproductive lifespan. Our analysis supports and extends previous findings, accounting for the possible confounding effects of other life history traits, ecological and dietary factors, and phylogenetic autocorrelation. Thus, these findings provide support for the hypothesis that mammals counterbalance the costs of affording large brains with a longer reproductive life.     

Large‐brained birds suffer less oxidative damage

Large brains (relative to body size) might confer fitness benefits to animals. Although the putative costs of well‐developed brains can constrain the majority of species to modest brain sizes, these costs are still poorly understood. Given that the neural tissue is energetically expensive and demands antioxidants, one potential cost of developing and maintaining large brains is increased oxidative stress (‘oxidation exposure’ hypothesis). Alternatively, because large‐brained species exhibit slow‐paced life histories, they are expected to invest more into self‐maintenance such as an efficacious antioxidative defence machinery (‘oxidation avoidance’ hypothesis). We predict decreased antioxidant levels and/or increased oxidative damage in large‐brained species in case of oxidation exposure, and the contrary in case of oxidation avoidance. We address these contrasting hypotheses for the first time by means of a phylogenetic comparative approach based on an unprecedented data set of four redox state markers from 85 European bird species. Large‐brained birds suffered less oxidative damage to lipids (measured as malondialdehyde levels) and exhibited higher total nonenzymatic antioxidant capacity than small‐brained birds, whereas uric acid and glutathione levels were independent of brain size. These results were not altered by potentially confounding variables and did not depend on how relative brain size was quantified. Our findings partially support the ‘oxidation avoidance’ hypothesis and provide a physiological explanation for the linkage of large brains with slow‐paced life histories: reduced oxidative stress of large‐brained birds can secure brain functionality and healthy life span, which are integral to their lifetime fitness and slow‐paced life history.     

Larger brain size indirectly increases vulnerability to extinction in mammals

Although previous studies have addressed the question of why large brains evolved, we have limited understanding of potential beneficial or detrimental effects of enlarged brain size in the face of current threats. Using novel phylogenetic path analysis, we evaluated how brain size directly and indirectly, via its effects on life history and ecology, influences vulnerability to extinction across 474 mammalian species. We found that larger brains, controlling for body size, indirectly increase vulnerability to extinction by extending the gestation period, increasing weaning age, and limiting litter sizes. However, we found no evidence of direct, beneficial, or detrimental effects of brain size on vulnerability to extinction, even when we explicitly considered the different types of threats that lead to vulnerability. Order‐specific analyses revealed qualitatively similar patterns for Carnivora and Artiodactyla. Interestingly, for Primates, we found that larger brain size was directly (and indirectly) associated with increased vulnerability to extinction. Our results indicate that under current conditions, the constraints on life history imposed by large brains outweigh the potential benefits, undermining the resilience of the studied mammals. Contrary to the selective forces that have favored increased brain size throughout evolutionary history, at present, larger brains have become a burden for mammals.     

Brain size predicts the success of mammal species introduced into novel environments

Large brains, relative to body size, can confer advantages to individuals in the form of behavioral flexibility. Such enhanced behavioral flexibility is predicted to carry fitness benefits to individuals facing novel or altered environmental conditions, a theory known as the brain size-environmental change hypothesis. Here, we provide the first empirical link between brain size and survival in novel environments in mammals, the largest-brained animals on Earth. Using a global database documenting the outcome of more than 400 introduction events, we show that mammal species with larger brains, relative to their body mass, tend to be more successful than species with smaller brains at establishing themselves when introduced to novel environments, when both taxonomic and regional autocorrelations are accounted for. This finding is robust to the effect of other factors known to influence establishment success, including introduction effort and habitat generalism. Our results replicate similar findings in birds, increasing the generality of evidence for the idea that enlarged brains can provide a survival advantage in novel environments.     

Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles

Brain size relative to body size varies considerably among animals, but the ecological consequences of that variation remain poorly understood. Plausibly, larger brains confer increased behavioural flexibility, and an ability to respond to novel challenges. In keeping with that hypothesis, successful invasive species of birds and mammals that flourish after translocation to a new area tend to have larger brains than do unsuccessful invaders. We found the same pattern in ectothermic terrestrial vertebrates. Brain size relative to body size was larger in species of amphibians and reptiles reported to be successful invaders, compared to species that failed to thrive after translocation to new sites. This pattern was found in six of seven global biogeographic realms; the exception (where relatively larger brains did not facilitate invasion success) was Australasia. Establishment success was also higher in amphibian and reptile families with larger relative brain sizes. Future work could usefully explore whether invasion success is differentially associated with enlargement of specific parts of the brain (as predicted by the functional role of the forebrain in promoting behavioural flexibility), or with a general size increase (suggesting that invasion success is facilitated by enhanced perceptual and motor skills, as well as cognitive ability).     

Resource availability modulates the effect of body size on reproductive development

Within-species variation in animal body size predicts major differences in life history, for example, in reproductive development, fecundity, and even longevity. Purely from an energetic perspective, large size could entail larger energy reserves, fuelling different life functions, such as reproduction and survival (the “energy reserve” hypothesis). Conversely, larger body size could demand more energy for maintenance, and larger individuals might do worse in reproduction and survival under resource shortage (the “energy demand” hypothesis). Disentangling these alternative hypotheses is difficult because large size often correlates with better resource availability during growth, which could mask direct effects of body size on fitness traits. Here, we used experimental body size manipulation in the freshwater cnidarian Hydra oligactis, coupled with manipulation of resource (food) availability to separate direct effects of body size from resource availability on fitness traits (sexual development time, fecundity, and survival). We found significant interaction between body size and food availability in sexual development time in both males and females, such that large individuals responded less strongly to variation in resource availability. These results are consistent with an energy reserve effect of large size in Hydra. Surprisingly, the response was different in males and females: small and starved females delayed their reproduction, while small and starved males developed reproductive organs faster. In case of fecundity and survival, both size and food availability had significant effects, but we detected no interaction between them. Our observations suggest that in Hydra, small individuals are sensitive to fluctuations in resource availability, but these small individuals are able to adjust their reproductive development to maintain fitness.     

Sociality, ecology, and relative brain size in lemurs

The social brain hypothesis proposes that haplorhine primates have evolved relatively large brains for their body size primarily as an adaptation for living in complex social groups. Studies that support this hypothesis have shown a strong relationship between relative brain size and group size in these taxa. Recent reports suggest that this pattern is unique to haplorhine primates; many nonprimate taxa do not show a relationship between group size and relative brain size. Rather, pairbonded social monogamy appears to be a better predictor of a large relative brain size in many nonprimate taxa. It has been suggested that haplorhine primates may have expanded the pairbonded relationship beyond simple dyads towards the evolution of complex social groups. We examined the relationship between group size, pairbonding, and relative brain size in a sample of 19 lemurs; strepsirrhine primates that last share a common ancestor with monkeys and apes approximately 75 Ma. First, we evaluated the social brain hypothesis, which predicts that species with larger social groups will have relatively larger brains. Secondly, we tested the pairbonded hypothesis, which predicts that species with a pairbonded social organization will have relatively larger brains than non-pairbonded species. We found no relationship between group size or pairbonding and relative brain size in lemurs. We conducted two further analyses to test for possible relationships between two nonsocial variables, activity pattern and diet, and relative brain size. Both diet and activity pattern are significantly associated with relative brain size in our sample. Specifically, frugivorous species have relatively larger brains than folivorous species, and cathemeral species have relatively larger brains than diurnal, but not nocturnal species. These findings highlight meaningful differences between Malagasy strepsirrhines and haplorhines, and between Malagasy strepsirrhines and nonprimate taxa, regarding the social and ecological factors associated with increases in relative brain size. The results suggest that factors such as foraging complexity and flexibility of activity patterns may have driven selection for increases in brain size in lemurs.     

Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutta)

The basis for our knowledge of brain evolution in vertebrates rests heavily on empirical evidence from comparative studies at the species level. However, little is still known about the natural levels of variation and the evolutionary causes of differences in brain size and brain structure within‐species, even though selection at this level is an important initial generator of macroevolutionary patterns across species. Here, we examine how early life‐history decisions and sex are related to brain size and brain structure in wild populations using the existing natural variation in mating strategies among wild brown trout (Salmo trutta). By comparing the brains of precocious fish that remain in the river and sexually mature at a small size with those of migratory fish that migrate to the sea and sexually mature at a much larger size, we show, for the first time in any vertebrate, strong differences in relative brain size and brain structure across mating strategies. Precocious fish have larger brain size (when controlling for body size) but migratory fish have a larger cerebellum, the structure in charge of motor coordination. Moreover, we demonstrate sex‐specific differences in brain structure as female precocious fish have a larger brain than male precocious fish while males of both strategies have a larger telencephalon, the cognitive control centre, than females. The differences in brain size and structure across mating strategies and sexes thus suggest the possibility for fine scale adaptive evolution of the vertebrate brain in relation to different life histories.     

Large‐brained frogs mature later and live longer

Brain sizes vary substantially across vertebrate taxa, yet, the evolution of brain size appears tightly linked to the evolution of life histories. For example, larger brained species generally live longer than smaller brained species. A larger brain requires more time to grow and develop at a cost of exceeded gestation period and delayed weaning age. The cost of slower development may be compensated by better homeostasis control and increased cognitive abilities, both of which should increase survival probabilities and hence life span. To date, this relationship between life span and brain size seems well established in homoeothermic animals, especially in mammals. Whether this pattern occurs also in other clades of vertebrates remains enigmatic. Here, we undertake the first comparative test of the relationship between life span and brain size in an ectothermic vertebrate group, the anuran amphibians. After controlling for the effects of shared ancestry and body size, we find a positive correlation between brain size, age at sexual maturation, and life span across 40 species of frogs. Moreover, we also find that the ventral brain regions, including the olfactory bulbs, are larger in long‐lived species. Our results indicate that the relationship between life history and brain evolution follows a general pattern across vertebrate clades.     

Encephalization and the evolution of longevity in mammals

Allometric principles account for most of the observed variation in maximum life span among mammals. When body-size effects are controlled for, most of the residual variance in mammalian life span can be explained by variations in brain size, metabolic rate and body temperature. It is shown that species with large brains for a given body size and metabolic rate, such as anthropoid primates, also have long maximum life spans. Conversely, mammals with relatively high metabolic rates and low levels of encephalization, as in most insectivores and rodents, tend to have short life spans. The hypothesis is put forward that encephalization and metabolic rate, which may govern other life history traits, such as growth and reproduction, are the primary determinants directing the evolution of mammalian longevity.     

Life history variation in Barents Sea fish: implications for sensitivity to fishing in a changing environment

• Under exploitation and environmental change, it is essential to assess the sensitivity and vulnerability of marine ecosystems to such stress. A species' response to stress depends on its life history. Sensitivity to harvesting is related to the life history “fast–slow” continuum, where “slow” species (i.e., large, long lived, and late maturing) are expected to be more sensitive to fishing than “fast” ones. We analyze life history traits variation for all common fish species in the Barents Sea and rank fishes along fast–slow gradients obtained by ordination analyses. In addition, we integrate species' fast–slow ranks with ecosystem survey data for the period 2004–2009, to assess life history variation at the community level in space and time. Arctic fishes were smaller, had shorter life spans, earlier maturation, larger offspring, and lower fecundity than boreal ones. Arctic fishes could thus be considered faster than the boreal species, even when body size was corrected for. Phylogenetically related species possessed similar life histories. Early in the study period, we found a strong spatial gradient, where members of fish assemblages in the southwestern Barents Sea displayed slower life histories than in the northeast. However, in later, warmer years, the gradient weakened caused by a northward movement of boreal species. As a consequence, the northeast experienced increasing proportions of slower fish species. This study is a step toward integrating life history traits in ecosystem‐based areal management. On the basis of life history traits, we assess the fish sensitivity to fishing, at the species and community level. We show that climate warming promotes a borealization of fish assemblages in the northeast, associated with slower life histories in that area. The biology of Arctic species is still poorly known, and boreal species that now establish in the Arctic are fishery sensitive, which calls for cautious ecosystem management of these areas.

     

Digest: A synergistic approach explains the evolutionary connection between brain size and longevity*

The cognitive buffer hypothesis poses that brain size evolves to buffer individuals from environmental changes, increasing survival. Jiménez-Ortega et al. (2020) explored this hypothesis using a phylogenetic path analysis and showed that there is a direct causal link between brain size and longevity in birds, even when allometric effects are taken into account. Furthermore, a synergistic model was better supported than models that included independent effects of brain size and body size.     

Effects of Life Histories on Genome Size Variation in Squamata

Genome size changes significantly among taxonomic levels, and this variation is often related to the patterns shaped by the phylogeny, life histories and ecological factors. However, there are mixed evidences on the main factors affecting molecular evolution in animals.In this study, we used phylogenetic comparative analysis to investigate the evolutionary rate of genome size and the relationships between genome size and life histories(i.e.,hatchling mass, clutch size, clutches per year, age at sexual maturity, lifespan and body mass) among 199 squamata species. Our results showed that the evolutionary rate of genome size in Lacertilia was significantly faster than Serpentes. Moreover, we also found that larger species showed larger hatchling mass, more clutches per year and clutch size and longer lifespan. However, genome size was negatively associated with clutch size and clutches per year, but not associated with body mass we looked at.The findings suggest that larger species do not possess the evolution of large genomes in squamata.     

Delphinid brain development from neonate to adulthood with comparisons to other cetaceans and artiodactyls

Why do neonatal and adult delphinids have much larger brains than artiodactyls when they have common ancestors? We explore relationships between neonatal brain size, gestation duration, maternal body mass, and body growth. Cetacean brains grow fast in the womb and longer gestation results in a larger brain. Allometry shows that the larger the mother's body mass, the larger the neonatal brain. After birth, delphinid bodies grow much faster than brains, and the index of encephalization decreases even as brains grow beyond maturity. Delphinids’ larger brain growth during life at sea may be explained by at least three differences from artiodactyls’ life on land. First, the sea offers high calorie prey to support growth of a large brain. Second, life in water offers relief from gravity, allowing for a large head to contain a large brain. Third, sound in water may pass through an immersed body. This allows sounds from the water to reach the fetus, driving early development of delphinoid auditory brain parts. As an example of this, the dolphin ear bone is very large at birth. Furthermore, the auditory nervous system appears mature well before birth. Compared with artiodactyls, these three differences likely result in a larger delphinid brain.     

Do smart birds stress less? An interspecific relationship between brain size and corticosterone levels

Vertebrates respond to unpredictable noxious environmental stimuli by increasing secretion of glucocorticoids (CORT). Although this hormonal stress response is adaptive, high levels of CORT may induce significant costs if stressful situations are frequent. Thus, alternative coping mechanisms that help buffer individuals against environmental stressors may be selected for when the costs of CORT levels are elevated. By allowing individuals to identify, anticipate and cope with the stressful circumstances, cognition may enable stress-specific behavioural coping. Although there is evidence that behavioural responses allow animals to cope with stressful situations, it is unclear whether or not cognition reduces investment in the neuroendocrine stress response. Here, we report that in birds, species with larger brains relative to their body size show lower baseline and peak CORT levels than species with smaller brains. This relationship is consistent across life-history stages, and cannot be accounted for by differences in life history and geographical latitude. Because a large brain is a major feature of birds that base their lifetime in learning new things, our results support the hypothesis that enhanced cognition represents a general alternative to the neuroendocrine stress response.