Trajectories and Constraints in Brain Evolution in Primates and Cetaceans

A negative allometric relationship between body mass (BM) and brain size (BS) can be observed for many vertebrate groups. In the past decades, researchers have proposed several hypotheses to explain this finding, but none is definitive and some are possibly not mutually exclusive. Certain species diverge markedly (positively or negatively) from the mean of the ratio BM/BS expected for a particular taxonomic group. It is possible to define encephalization quotient (EQ) as the ratio between the actual BS and the expected brain size. Several cetacean species show higher EQs compared to all primates, except modern humans. The process that led to big brains in primates and cetaceans produced different trajectories, as shown by the organizational differences observed in every encephalic district (e.g., the cortex). However, these two groups both convergently developed complex cognitive abilities. The comparative study on the trajectories through which the encephalization process has independently evolved in primates and cetaceans allows a critical appraisal of the causes, the time and the mode of quantitative and qualitative development of the brain in our species and in the hominid evolutionary lineage.     

Tool use, aye-ayes, and sensorimotor intelligence

Humans, chimpanzees, capuchins and aye-ayes all display an unusually high degree of encephalization and diverse omnivorous extractive foraging. It has been suggested that the high degree of encephalization in aye-ayes may be the result of their diverse, omnivorous extractive foraging behaviors. In combination with certain forms of tool use, omnivorous extractive foraging has been hypothesized to be linked to higher levels of sensorimotor intelligence (stages 5 or 6). Although free-ranging aye-ayes have not been observed to use tools directly in the context of their extractive foraging activities, they have recently been reported to use lianas as tools in a manner that independently suggests that they may possess stage 5 or 6 sensorimotor intelligence. Although other primate species which display diverse, omnivorous extractive foraging have been tested for sensorimotor intelligence, aye-ayes have not. We report a test of captive aye-ayes' comprehension of tool use in a situation designed to simulate natural conditions. The results support the view that aye-ayes do not achieve stage 6 comprehension of tool use, but rather may use trial-and-error learning to develop tool-use behaviors. Other theories for aye-aye encephalization are considered.     

Encephalization in Gobioidei (Teleostei)

We have measured the brain and body weight and determined the encephalization index for 180 species of fishes belonging to six families of the suborder Gobioidei. Within the Teleostei, these fishes exhibit a remarkably broad range in the values of their encephalization indices, but most values are in the low to middle range. Within the Gobioidei there is relatively little difference in the degree of encephalization among the different families and subfamilies except the Kraemeriidae and Amblyopinae which have low encephalization indices and the Oxudercinae (including Periophthalmus) and Rhyacichthyidae which are highly encephalized. We have shown that the form of the body has an effect on the degree of encephalization. Elongate fishes have low values, probably because of the excessive mass of their body skeleton which raises the body weight relative to the brain size. The environment in which the fishes live is correlated, in general, with their relative brain size. The values of the encephalization index arranged from low to high by habitat are as follows: muddwelling fishes, freshwater fishes, brackishwater fishes, burrowing marine fishes, freeliving marine fishes, torrent fishes and amphibious fishes. The low values of the Amblyopinae and Kraemeriidae can be explained in terms of their being both mud-dwelling and elongate.     

On the evolution of brain size in relation to migratory behaviour in birds

Migratory birds appear to have relatively smaller brain size compared to sedentary species. It has been hypothesized that initial differences in brain size underlying behavioural flexibility drove the evolution of migratory behaviour; birds with relatively large brains evolved sedentary habits and those with relatively small brains evolved migratory behaviour (migratory precursor hypothesis). Alternative hypotheses suggest that changes in brain size might follow different behavioural strategies and that sedentary species might have evolved larger brains because of differences in selection pressures on brain size in migratory and nonmigratory species. Here we present the first evidence arguing against the migratory precursor hypothesis. We compared relative brain volume of three subspecies of the white-crowned sparrow: sedentary Zonotrichia leucophrys nuttalli and migratory Z. l. gambelii and Z. l. oriantha. Within the five subspecies of the white-crowned sparrow, only Z. l. nuttalli is strictly sedentary. The sedentary behaviour of Z. l. nuttalli is probably a derived trait, because Z. l. nuttalli appears to be the most recent subspecies and because all species ancestral to Zonotrichia as well as all older subspecies of Z. leucophrys are migratory. Compared to migratory Z. l. gambelii and Z. l. oriantha, we found that sedentary Z. l. nuttalli had a significantly larger relative brain volume, suggesting that the larger brain of Z. l. nuttalli evolved after a switch to sedentary behaviour. Thus, in this group, brain size does not appear to be a precursor to the evolution of migratory or sedentary behaviour but rather an evolutionary consequence of a change in migratory strategy.     

Feeding Responses of Hatchery-Reared Gilthead Sea Bream (Sparus aurata L.) to a Commercial Diet and Natural Prey Items

Many fish species have evolved feeding mechanisms and behaviours enabling them to feed on specific prey. However, such mechanisms may not be optimal for feeding on commercial-pelleted diets in aquaculture. Gilthead sea bream chew and occasionally eject pellets or parts of pellets from the mouth when feeding on commercial diets. This may result in an increase in nutritional waste from the intensive culture of this species. In this study we examined the prevalence of this food processing behaviour in two sizes of sea bream, feeding on three types of natural prey items in comparison to a commercial pellet, to give an insight into the circumstances in which excess chewing and ejection of food items from the mouth occurred. These included two hard-textured food items (commercial pellet and hard-shelled prey) and two soft-textured food items (larvae and small crustacean). Both sizes of sea bream frequently consumed the soft-textured food types, however large sea bream also frequently consumed hard-textured pellets. Hard-textured food required longer handling times and elicited more chewing and the ejection of food items from the mouth. These results suggest that future investigations on the food processing behaviour and consequent waste when fed commercial diets differing in texture could give an insight into improving diets and feeding efficiency for intensively cultivated gilthead sea bream.     

Feeding Responses of Hatchery-Reared Gilthead Sea Bream (Sparus aurata L.) to a Commercial Diet and Natural Prey Items

Many fish species have evolved feeding mechanisms and behaviours enabling them to feed on specific prey. However, such mechanisms may not be optimal for feeding on commercial-pelleted diets in aquaculture. Gilthead sea bream chew and occasionally eject pellets or parts of pellets from the mouth when feeding on commercial diets. This may result in an increase in nutritional waste from the intensive culture of this species. In this study we examined the prevalence of this food processing behaviour in two sizes of sea bream, feeding on three types of natural prey items in comparison to a commercial pellet, to give an insight into the circumstances in which excess chewing and ejection of food items from the mouth occurred. These included two hard-textured food items (commercial pellet and hard-shelled prey) and two soft-textured food items (larvae and small crustacean). Both sizes of sea bream frequently consumed the soft-textured food types, however large sea bream also frequently consumed hard-textured pellets. Hard-textured food required longer handling times and elicited more chewing and the ejection of food items from the mouth. These results suggest that future investigations on the food processing behaviour and consequent waste when fed commercial diets differing in texture could give an insight into improving diets and feeding efficiency for intensively cultivated gilthead sea bream.     

Increased brain size in mammals is associated with size variations in gene families with cell signalling,chemotaxis and immune-related functions

Genomic determinants underlying increased encephalization across mammalian lineages are unknown. Whole genome comparisons have revealed large and frequent changes in the size of gene families, and it has been proposed that these variations could play a major role in shaping morphological and physiological differences among species. Using a genome-wide comparative approach, we examined changes in gene family size (GFS) and degree of encephalization in 39 fully sequenced mammalian species and found a significant over-representation of GFS variations in line with increased encephalization in mammals. We found that this relationship is not accounted for by known correlates of brain size such as maximum lifespan or body size and is not explained by phylogenetic relatedness. Genes involved in chemotaxis, immune regulation and cell signalling-related functions are significantly over-represented among those gene families most highly correlated with encephalization. Genes within these families are prominently expressed in the human brain, particularly the cortex, and organized in co-expression modules that display distinct temporal patterns of expression in the developing cortex. Our results suggest that changes in GFS associated with encephalization represent an evolutionary response to the specific functional requirements underlying increased brain size in mammals.     

Neuroecology of cartilaginous fishes: the functional implications of brain scaling

It is a widely accepted view that neural development can reflect morphological adaptations and sensory specializations. The aim of this review is to give a broad overview of the current status of brain data available for cartilaginous fishes and examine how perspectives on allometric scaling of brain size across this group of fishes has changed within the last 50 years with the addition of new data and more rigorous statistical analyses. The current knowledge of neuroanatomy in cartilaginous fishes is reviewed and data on brain size (encephalization, n = 151) and interspecific variation in brain organization (n = 84) has been explored to ascertain scaling relationships across this clade. It is determined whether similar patterns of brain organization, termed cerebrotypes, exist in species that share certain lifestyle characteristics. Clear patterns of brain organization exist across cartilaginous fishes, irrespective of phylogenetic grouping and, although this study was not a functional analysis, it provides further evidence that chondrichthyan brain structures might have developed in conjunction with specific behaviours or enhanced cognitive capabilities. Larger brains, with well-developed telencephala and large, highly foliated cerebella are reported in species that occupy complex reef or oceanic habitats, potentially identifying a reef-associated cerebrotype. In contrast, benthic and benthopelagic demersal species comprise the group with the smallest brains, with a relatively reduced telencephalon and a smooth cerebellar corpus. There is also evidence herein of a bathyal cerebrotype; deep-sea benthopelagic sharks possess relatively small brains and show a clear relative hypertrophy of the medulla oblongata. Despite the patterns observed and documented, significant gaps in the literature have been highlighted. Brain mass data are only currently available on c. 16% of all chondrichthyan species, and only 8% of species have data available on their brain organization, with far less on subsections of major brain areas that receive distinct sensory input. The interspecific variability in brain organization further stresses the importance of performing functional studies on a greater range of species. Only an expansive data set, comprised of species that span a variety of habitats and taxonomic groups, with widely disparate behavioural repertoires, combined with further functional analyses, will help shed light on the extent to which chondrichthyan brains have evolved as a consequence of behaviour, habitat and lifestyle in addition to phylogeny.     

Endocranial Volume of Mid-Late Eocene Archaeocetes (Order: Cetacea) Revealed by Computed Tomography: Implications for Cetacean Brain Evolution

The large brain of modern cetaceans has engendered much hypothesizing about both the intelligence of cetaceans (dolphins, whales, and porpoises) and the factors related to the evolution of such large brains. Despite much interest in cetacean brain evolution, until recently there have been few estimates of brain mass and/or brain–body weight ratios in fossil cetaceans. In the present study, computed tomography (CT) was used to visualize and estimate endocranial volume, as well as to calculate level of encephalization, for two fully aquatic mid-late Eocene archaeocete species, Dorudon atrox and Zygorhiza kochii. The specific objective was to address more accurately and more conclusively the question of whether relative brain size in fully aquatic archaeocetes was greater than that of their hypothesized sister taxon Mesonychia. The findings suggest that there was no increase in encephalization between Mesonychia and these archaeocete species.     

Experimental evolution of a microbial predator's ability to find prey

Foraging theory seeks to explain how the distribution and abundance of prey influence the evolution of predatory behaviour, including the allocation of effort to searching for prey and handling them after they are found. While experiments have shown that many predators alter their behaviour phenotypically within individual lifetimes, few have examined the actual evolution of predatory behaviour in light of this theory. Here, we test the effects of prey density on the evolution of a predator's searching and handling behaviours using a bacterial predator, Myxococcus xanthus. Sixteen predator populations evolved for almost a year on agar surfaces containing patches of Escherichia coli prey at low or high density. Improvements in searching rate were significantly greater in those predators that evolved at low prey density. Handling performance also improved in some predator populations, but prey density did not significantly affect the magnitude of these gains. As the predators evolved greater foraging proficiency, their capacity diminished to produce fruiting bodies that enable them to survive prolonged periods of starvation. More generally, these results demonstrate that predators evolve behaviours that reflect at least some of the opportunities and limitations imposed by the distribution and abundance of their prey.     

Neural mechanisms underlying the evolvability of behaviour

The complexity of nervous systems alters the evolvability of behaviour. Complex nervous systems are phylogenetically constrained; nevertheless particular species-specific behaviours have repeatedly evolved, suggesting a predisposition towards those behaviours. Independently evolved behaviours in animals that share a common neural architecture are generally produced by homologous neural structures, homologous neural pathways and even in the case of some invertebrates, homologous identified neurons. Such parallel evolution has been documented in the chromatic sensitivity of visual systems, motor behaviours and complex social behaviours such as pair-bonding. The appearance of homoplasious behaviours produced by homologous neural substrates suggests that there might be features of these nervous systems that favoured the repeated evolution of particular behaviours. Neuromodulation may be one such feature because it allows anatomically defined neural circuitry to be re-purposed. The developmental, genetic and physiological mechanisms that contribute to nervous system complexity may also bias the evolution of behaviour, thereby affecting the evolvability of species-specific behaviour.     

Cognitive ornithology: the evolution of avian intelligence

Comparative psychologists interested in the evolution of intelligence have focused their attention on social primates, whereas birds tend to be used as models of associative learning. However, corvids and parrots, which have forebrains relatively the same size as apes, live in complex social groups and have a long developmental period before becoming independent, have demonstrated ape-like intelligence. Although, ornithologists have documented thousands of hours observing birds in their natural habitat, they have focused their attention on avian behaviour and ecology, rather than intelligence. This review discusses recent studies of avian cognition contrasting two different approaches; the anthropocentric approach and the adaptive specialization approach. It is argued that the most productive method is to combine the two approaches. This is discussed with respects to recent investigations of two supposedly unique aspects of human cognition; episodic memory and theory of mind. In reviewing the evidence for avian intelligence, corvids and parrots appear to be cognitively superior to other birds and in many cases even apes. This suggests that complex cognition has evolved in species with very different brains through a process of convergent evolution rather than shared ancestry, although the notion that birds and mammals may share common neural connectivity patterns is discussed.     

Relationship between morphology,dispersal and habitat distribution in three species of Libellula (Odonata: Anisoptera)

Morphology is an important determinant of flight performance and can shape species’ dispersal behaviour. This study contrasted the morphology of flight-related structures in dragonfly species with different dispersal behaviours to gain insights into the relationship between morphology and dispersal behaviour. Specifically, wing size, wing shape and thorax size were compared in three co-occurring species from different clades within the genus Libellula (Odonata: Anisoptera: Libellulidae) to assess how these morphological traits are related to differences in dispersal behaviour and to how broadly their larvae occur across a habitat gradient. Two species had broad larval habitat distributions as well as high rates and distances of dispersal. These two species had relatively larger wings and thoraces than the third species, which was found only in permanent lakes and had limited dispersal. The hind-wings of more dispersive species also had lower aspect ratios and a relatively wider basal portion of the wing than the less dispersive species. Broad hind-wings may facilitate the use of gliding flight and reduce the energetic costs of dispersal. Determining the morphological traits associated with alternative dispersal behaviours may be a useful tool to assess the differential dispersal capacities of species or populations.     

The evolution of animal 'cultures' and social intelligence

Decades-long field research has flowered into integrative studies that, together with experimental evidence for the requisite social learning capacities, have indicated a reliance on multiple traditions ('cultures') in a small number of species. It is increasingly evident that there is great variation in manifestations of social learning, tradition and culture among species, offering much scope for evolutionary analysis. Social learning has been identified in a range of vertebrate and invertebrate species, yet sustained traditions appear rarer, and the multiple traditions we call cultures are rarer still. Here, we examine relationships between this variation and both social intelligence--sophisticated information processing adapted to the social domain--and encephalization. First, we consider whether culture offers one particular confirmation of the social ('Machiavellian') intelligence hypothesis that certain kinds of social life (here, culture) select for intelligence: 'you need to be smart to sustain culture'. Phylogenetic comparisons, particularly focusing on our own study animals, the great apes, support this, but we also highlight some paradoxes in a broader taxonomic survey. Second, we use intraspecific variation to address the converse hypothesis that 'culture makes you smart', concluding that recent evidence for both chimpanzees and orangutans support this proposition.     

Nouvelles données sur 'encéphalisation des Reptiles Squamates

New datas on the level of encephalization of Squamate Reptiles This study carried out on 32 species of Lizards, 15 species of Snakes and one Amphisbaenian, the measure of the brain-weight (Brw) and the body-weight (Bdw) of which leads to the determination of the a and k parameters of the SNEL'S formula: Brw =k– Bdw^α. In a first stage we are able to demonstrate with 9 species of Saurians and 2 species of Ophidians, each species being represented by a sample the size of which variing between 30 to 80, that the intrinsic variability of the brain gives a mean value of 6.4% (isoponderal variability) or 7.5% (isometric variability). The intraspecific α coefficients (allometric coefficients of growth or of size) remain between.383 and.500; the mean value of which, .43 will be considered as a characteristic of the order Squamata. The interspecific α. coefficient (filiation coefficient of BAUCHOT and PLATEL) given by the 32 species of Lizards is .669, quite close to those previously calculated from a sample of 23 species (.686). The former values of the indices of encephalization belonging to these 23 species are meanwhile different. Six Lacertidae, selected as referrence Saurians (α= 627) lead to new indices of encephalization, the value of which will not be henceforth altered by the addition of new species to our present sample of Saurians. The various adaptative peculiarities roughly expressed by these indices of encephalization will be shortly studied in detail by the way of the volumetric analysis of the nuclear components of the brain. Amongst the 15 Snakes, the discrimination of 3 Henophidians and 12 Caenophidians leads for the last ones to an a filiation coefficient of .664; the value found for the Henophidians (.750) must be considered with suspicion because it get from only 3 species. We find with Anguis, the Amphisbaenian, some Scincidae and all the Snakes a low level of encephalization linked to the legless condition, which masks perhaps another peculiarities related to the evolutive processus which leads from Lizards to Snakes. The analyses of the K/Bdw relationship leads to results which differ from those found by BAUCHOT with the Insectivores-Primates. Separately Saurians and Ophidians do not show any correlation between the coefficient of encephalization and the body-weight; in compensation the Squamata in a whole show characteristics which express a negative rate of encephalization.     

Sexual signalling in female crested macaques and the evolution of primate fertility signals

ABSTRACT: BACKGROUND: Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females' interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour. RESULTS: We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this. CONCLUSION: Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.     

Biphasic Retention of One-Trial Learning in a Clonal Fish (<Emphasis Type="Italic">Poecilia formosa</Emphasis>)

Most species used for behavioural studies are bisexual. Sexual dimorphism determines genotypic diversity and behavioural variation within a species. The relative contribution of a genome to a specific behaviour is for the most part indiscernible, but gene changes can alter behaviour in many different ways¹. Within a species, strain differences can contribute to behavioural differences and many less clearly systematic behaviours, such as the aptitude to learn or to recall, may be genetically determined². Genotypic diversity, on the other hand, obscures gene correlates of behaviour because each organism brings a unique repertoire of behaviours to the experimental situation. Against this, learning research has found basic phenomena of learning and memory to be valid across many vertebrate species. In an effort to reduce genotypic and behavioural variability in studying memory processing, we have used a unisexual clonal fish, Poecilia formosa, as suggested by Agranoff and Davis³.     

The odour makes the difference: male moths attracted by sex pheromones ignore the threat by predatory bats

How animals adjust their foraging or mate finding behaviour according to the risk of predation has received much attention recently. However, few studies have focused on the behaviour of prey when stimuli representing different adaptive behaviours originate from different sensory modalities. Here we present data on how male moths trade off odour-mediated mate attraction and auditory-mediated predator avoidance depending on the relative quality of the mate signal. Males of Agrotis segetum (Noctuidae) and Plodia interpunctella (Pyralidae), orienting towards a sex pheromone source in a flight tunnel, were exposed to ultrasound mimicking the echolocation calls of a bat, i.e. high predation risk. Males of both species accepted the predation risk when attracted to pheromone sources of high quality (female gland extract or complete synthetic blend at high dose), manifested in similar percentages reaching the pheromone source in moths with and without ultrasound exposure. In contrast, a lower proportion of ultrasound-exposed males than unexposed ones located the pheromone source when moths were flying towards pheromone sources of low quality (incomplete synthetic blend or complete synthetic blend at low dose), due to more time invested in defence manoeuvres. Furthermore, the risk taking behaviours of these moth species seem to be similar in spite of the fact that their ultrasonic hearing systems have evolved independently.     

THE EVOLUTIONARY HISTORY OF CETACEAN BRAIN AND BODY SIZE

Cetaceans rival primates in brain size relative to body size and include species with the largest brains and biggest bodies to have ever evolved. Cetaceans are remarkably diverse, varying in both phenotypes by several orders of magnitude, with notable differences between the two extant suborders, Mysticeti and Odontoceti. We analyzed the evolutionary history of brain and body mass, and relative brain size measured by the encephalization quotient (EQ), using a data set of extinct and extant taxa to capture temporal variation in the mode and direction of evolution. Our results suggest that cetacean brain and body mass evolved under strong directional trends to increase through time, but decreases in EQ were widespread. Mysticetes have significantly lower EQs than odontocetes due to a shift in brain:body allometry following the divergence of the suborders, caused by rapid increases in body mass in Mysticeti and a period of body mass reduction in Odontoceti. The pattern in Cetacea contrasts with that in primates, which experienced strong trends to increase brain mass and relative brain size, but not body mass. We discuss what these analyses reveal about the convergent evolution of large brains, and highlight that until recently the most encephalized mammals were odontocetes, not primates.     

The Ontogeny of Encephalization: Tradeoffs Between Brain Growth,Somatic Growth,and Life History in Hominoids and Platyrrhines

This study examines variation in brain growth relative somatic growth in four hominoids and three platyrrhines to determine whether there is a trade-off during ontogeny. I predicted that somatic growth would be reduced during periods of extensive brain growth, and species with larger degrees of encephalization would reach a smaller body size at brain growth completion because more energy is directed towards the brain. I measured cranial capacity and skeletal size in over 500 skeletal specimens from wild populations. I calculated nonlinear growth curves and velocity curves to determine brain/body growth allometry during ontogeny. In addition, I calculated linear regressions to describe the brain/body allometry during the postnatal period prior to brain size reaching an asymptote. The results showed that somatic growth is not substantially reduced in species with extensive brain growth, and body size at brain growth completion was larger in species with greater degrees of encephalization. Furthermore, large body size at brain growth completion was not correlated with interbirth interval, but was significantly correlated with prolonged juvenile periods and late age at maturity when data were corrected for phylogeny. These results indicate that neither reduction in body growth nor reproductive rate are compensatory mechanisms for the energetic costs of brain growth. Other avenues for meeting energetic costs must be in effect. In addition, the results show that somatic growth in encephalized species is particularly slow during the juvenile period after brain growth at or near completion, suggesting that these growth patterns are explained by reasons other than energetic costs.