Extended parental provisioning and variation in vertebrate brain sizes.

Large brains provide adaptive cognitive benefits but require unusually high, near-constant energy inputs and become fully functional well after their growth is completed. Consequently, young of most larger-brained endotherms should not be able to independently support the growth and development of their own brains. This paradox is solved if the evolution of extended parental provisioning facilitated brain size evolution. Comparative studies indeed show that extended parental provisioning coevolved with brain size and that it may improve immature survival. The major role of extended parental provisioning supports the idea that the ability to sustain the costs of brains limited brain size evolution.

A Farewell to the Encephalization Quotient: A New Brain Size Measure for Comparative Primate Cognition.

Both absolute and relative brain sizes vary greatly among and within the major vertebrate lineages. Scientists have long debated how larger brains in primates and hominins translate into greater cognitive performance, and in particular how to control for the relationship between the noncognitive functions of the brain and body size. One solution to this problem is to establish the slope of cognitive equivalence, i.e., the line connecting organisms with an identical bauplan but different body sizes. The original approach to estimate this slope through intraspecific regressions was abandoned after it became clear that it generated slopes that were too low by an unknown margin due to estimation error. Here, we revisit this method. We control for the error problem by focusing on highly dimorphic primate species with large sample sizes and fitting a line through the mean values for adult females and males. We obtain the best estimate for the slope of circa 0.27, a value much lower than those constructed using all mammal species and close to the value expected based on the genetic correlation between brain size and body size. We also find that the estimate of cognitive brain size based on cognitive equivalence fits empirical cognitive studies better than the encephalization quotient, which should therefore be avoided in future studies on primates and presumably mammals and birds in general. The use of residuals from the line of cognitive equivalence may change conclusions concerning the cognitive abilities of extant and extinct primate species, including hominins.

Gross intestinal morphometry and allometry in primates.

Although it is generally assumed that among mammals and within mammal groups, those species that rely on diets consisting of greater amounts of plant fiber have larger gastrointestinal tracts (GIT), statistical evidence for this simple claim is largely lacking. We compiled a dataset on the length of the small intestine, caecum, and colon in 42 strepsirrhine, platyrrhine, and catarrhine primate species, using specimens with known body mass (BM). We tested the scaling of intestine length with BM, and whether dietary proxies (percentage of leaves and a diet quality index) were significant covariates in these scaling relationships, using two sets of models: one that did not account for the phylogenetic structure of the data, and one that did. Intestine length mainly scaled geometrically at exponents that included 0.33 in the confidence interval; Strepsirrhini exhibited particularly long caeca, while those of Catarrhini were comparatively short. Diet proxies were only significant for the colon and the total large intestine (but not for the small intestine or the caecum), and only in conventional statistics (but not when accounting for phylogeny), indicating the pattern occurred across but not within clades. Compared to terrestrial Carnivora, primates have similar small intestine lengths, but longer large intestines. The data on intestine lengths presented here corroborate recent results on GIT complexity, suggesting that diet, as currently described, does not exhaustively explain GIT anatomy within primate clades.

Hibernation constrains brain size evolution in mammals.

The expensive brain hypothesis predicts that the lowest stable level of steady energy input acts as a strong constraint on a species' brain size, and thus, that periodic troughs in net energy intake should select for reduced brain size relative to body mass. Here, we test this prediction for the extreme case of hibernation. Hibernators drastically reduce food intake for up to several months and are therefore expected to have smaller relative brain sizes than nonhibernating species. Using a comparative phylogenetic approach on brain size estimates of 1104 mammalian species, and controlling for possible confounding variables, we indeed found that the presence of hibernation in mammals is correlated with decreased relative brain size. This result adds to recent comparative work across mammals and amphibians supporting the idea that environmental seasonality (where in extremis hibernation is necessary for survival) imposes an energetic challenge and thus acts as an evolutionary constraint on relative brain size.

Correction to: getting fat or getting help? how female mammals cope with energetic constraints on reproduction.

[This corrects the article DOI: 10.1186/s12983-017-0214-0.].

Getting fat or getting help? How female mammals cope with energetic constraints on reproduction.

BACKGROUND: Fat deposits enable a female mammal to bear the energy costs of offspring production and thus greatly influence her reproductive success. However, increasing locomotor costs and reduced agility counterbalance the fitness benefits of storing body fat. In species where costs of reproduction are distributed over other individuals such as fathers or non-breeding group members, reproductive females might therefore benefit from storing less energy in the form of body fat. RESULTS: Using a phylogenetic comparative approach on a sample of 87 mammalian species, and controlling for possible confounding variables, we found that reproductive females of species with allomaternal care exhibit reduced annual variation in body mass (estimated as CV body mass), which is a good proxy for the tendency to store body fat. Differential analyses of care behaviours such as allonursing or provisioning corroborated an energetic interpretation of this finding. The presumably most energy-intensive form of allomaternal care, provisioning of the young, had the strongest effect on CV body mass. In contrast, allonursing, which involves no additional influx of energy but distributes maternal help across different mothers, was not correlated with CV body mass. CONCLUSIONS: Our results suggest that reproducing females in species with allomaternal care can afford to reduce reliance on fat reserves because of the helpers' energetic contribution towards offspring rearing.

Being fat and smart: A comparative analysis of the fat-brain trade-off in mammals.

Humans stand out among non-aquatic mammals by having both an extremely large brain and a relatively large amount of body fat. To understand the evolution of this human peculiarity we report a phylogenetic comparative study of 120 mammalian species, including 30 primates, using seasonal variation in adult body mass as a proxy of the tendency to store fat. Species that rely on storing fat to survive lean periods are expected to be less active because of higher costs of locomotion and have increased predation risk due to reduced agility. Because a fat-storage strategy reduces the net cognitive benefit of a large brain without reducing its cost, such species should be less likely to evolve a larger brain than non-fat-storing species. We therefore predict that the two strategies to buffer food shortages (storing body fat and cognitive flexibility) are compensatory, and therefore predict negative co-evolution between relative brain size and seasonal variation in body mass. This trade-off is expected to be stronger in predominantly arboreal species than in more terrestrial ones, as the cost of transporting additional adipose depots is higher for climbing than for horizontal locomotion. We did, indeed, find a significant negative correlation between brain size and coefficient of variation (CV) in body mass in both sexes for the subsample of arboreal species, both in all mammals and within primates. In predominantly terrestrial species, in contrast, this correlation was not significant. We therefore suggest that the adoption of habitually terrestrial locomotor habits, accompanied by a reduced reliance on climbing, has allowed for a primate of our body size the unique human combination of unusually large brains and unusually large adipose depots.

The economics of brain size evolution in vertebrates.

Across the animal kingdom, we see remarkable variation in brain size. This variation has even increased over evolutionary time. Traditionally, studies aiming to explain brain size evolution have looked at the fitness benefits of increased brain size in relation to its increased cognitive performance in the social and/or ecological domain. However, brains are among the most energetically expensive tissues in the body and also require an uninterrupted energy supply. If not compensated, these energetic demands inevitably lead to a reduction in energy allocation to other vital functions. In this review, we summarize how an increasing number of studies show that to fully comprehend brain size evolution and the large variation in brain size across lineages, it is important to look at the economics of brains, including the different pathways through which the high energetic costs of brains can be offset. We further show how numerous studies converge on the conclusion that cognitive abilities can only drive brain size evolution in vertebrate lineages where they result in an improved energy balance through favourable ecological preconditions. Cognitive benefits that do not directly improve the organism's energy balance can only be selectively favoured when they produce such large improvements in reproduction or survival that they outweigh the negative energetic effects of the large brain.

Reproductive seasonality in primates: patterns, concepts and unsolved questions.

Primates, like other mammals, exhibit an annual reproductive pattern that ranges from strictly seasonal breeding to giving birth in all months of the year, but factors mediating this variation are not fully understood. We applied both a categorical description and quantitative measures of the birth peak breadth based on daily observations in zoos to characterise reproductive seasonality in 141 primate species with an average of 941 birth events per species. Absolute day length at the beginning of the mating season in seasonally reproducing species was not correlated between populations from natural habitats and zoos. The mid-point of latitudinal range was a major factor associated with reproductive seasonality, indicating a correlation with photoperiod. Gestation length, annual mean temperature, natural diet and Malagasy origin were other important factors associated with reproductive seasonality. Birth seasons were shorter with increasing latitude of geographical origin, corresponding to the decreasing length of the favourable season. Species with longer gestation periods were less seasonal than species with shorter ones, possibly because shorter gestation periods more easily facilitate the synchronisation of reproductive activity with annual cycles. Habitat conditions with higher mean annual temperature were also linked to less-seasonal reproduction, independently of the latitude effect. Species with a high percentage of leaves in their natural diet were generally non-seasonal, potentially because the availability of mature leaves is comparatively independent of seasons. Malagasy primates were more seasonal in their births than species from other regions. This might be due to the low resting metabolism of Malagasy primates, the comparatively high degree of temporal predictability of Malagasy ecosystems, or historical constraints peculiar to Malagasy primates. Latitudinal range showed a weaker but also significant association with reproductive seasonality. Amongst species with seasonal reproduction in their natural habitats, smaller primate species were more likely than larger species to shift to non-seasonal breeding in captivity. The percentage of species that changed their breeding pattern in zoos was higher in primates (30%) than in previous studies on Carnivora and Ruminantia (13 and 10%, respectively), reflecting a higher concentration of primate species in the tropics. When comparing only species that showed seasonal reproduction in natural habitats at absolute latitudes ≤11.75°, primates did not differ significantly from these two other taxa in the proportion of species that changed to a less-seasonal pattern in zoos. However, in this latitude range, natural populations of primates and Carnivora had a significantly higher proportion of seasonally reproducing species than Ruminantia, suggesting that in spite of their generally more flexible diets, both primates and Carnivora are more exposed to resource fluctuation than ruminants.

When ontogeny recapitulates phylogeny: Fixed neurodevelopmental sequence of manipulative skills among primates.

Neural development is highly conserved across distantly related species of different brain sizes. Here, we show that the development of manipulative complexity is equally cumulative across 36 primate species and also that its ontogeny recapitulates phylogeny. Furthermore, larger-brained species reach their adult skill levels later than smaller-brained ones, largely because they start later with the simplest techniques. These findings demonstrate that these motor behaviors are not modular and that their slow development may constrain their evolution. Complex foraging techniques therefore critically require a slow life history with low mortality, which explains the limited taxonomic distribution of flexible tool use and the unique elaboration of human technology.

Geographical Origin, Delayed Implantation, and Induced Ovulation Explain Reproductive Seasonality in the Carnivora.

Patterns of reproductive seasonality in the Carnivora are difficult to study comparatively, due to limited numbers of species for which information is available. Long-term databases of captive populations could overcome this difficulty. We apply a categorical description and a quantitative high-resolution measure (birth peak breadth, the number of days in which 80% of all births occur) based on daily observations in captivity to characterize the degree of reproductive seasonality in the Carnivora for 114 species with on average 1357 births per species. We find that the majority of species retained the birth seasonality displayed in the wild. Latitude of natural origin, delayed implantation, and induced ovulation were the main factors influencing reproductive seasonality. Most species were short-day breeders, but there was no evidence of an absolute photoperiodic signal for the timing of mating or conception. The length of the gestation period (corrected for body mass) generally decreased with birth seasonality but increased in species with delayed implantation. Birth seasons become shorter with increasing latitude of geographical origin, likely because the length of the favorable season declines with increasing latitude, exerting a strong selective pressure on fitting both the reproductive cycle and the interval offspring needs for growth following the termination of parental care into the short time window of optimal environmental conditions. Species with induced ovulation exhibit a less seasonal reproductive pattern, potentially because mates do not have to meet during a short time window of a fixed ovulation. Seasonal species of Carnivora shorten their gestation period so reproduction can occur during the short time window of optimal environmental conditions. Alternatively, other Carnivora species lengthen their gestation periods in order to bridge long winters. Interestingly, this occurs not by decelerating intrauterine growth but by delaying implantation.

Manipulation complexity in primates coevolved with brain size and terrestriality.

Humans occupy by far the most complex foraging niche of all mammals, built around sophisticated technology, and at the same time exhibit unusually large brains. To examine the evolutionary processes underlying these features, we investigated how manipulation complexity is related to brain size, cognitive test performance, terrestriality, and diet quality in a sample of 36 non-human primate species. We categorized manipulation bouts in food-related contexts into unimanual and bimanual actions, and asynchronous or synchronous hand and finger use, and established levels of manipulative complexity using Guttman scaling. Manipulation categories followed a cumulative ranking. They were particularly high in species that use cognitively challenging food acquisition techniques, such as extractive foraging and tool use. Manipulation complexity was also consistently positively correlated with brain size and cognitive test performance. Terrestriality had a positive effect on this relationship, but diet quality did not affect it. Unlike a previous study on carnivores, we found that, among primates, brain size and complex manipulations to acquire food underwent correlated evolution, which may have been influenced by terrestriality. Accordingly, our results support the idea of an evolutionary feedback loop between manipulation complexity and cognition in the human lineage, which may have been enhanced by increasingly terrestrial habits.