Evolution of the nose and nasal skeleton in primates

One traditional diagnostic feature of the Order Primates is a decreased emphasis on olfaction. 1 , 2 Some authors attribute this feature only to tarsiers and anthropoids, either through convergence or as a common feature of haplorhines. 2 - 4 Other authors de‐emphasize olfaction relative to vision, 5 - 7 which does not necessarily denote olfactory reduction per se. There are lengthy roots to this discussion. The importance of the sense of smell to at least some primates, humans in particular, has long been viewed as secondary to the importance of visual, auditory, and tactile senses. Smell, or olfaction, is viewed as the primitive special sense, the stimuli perceived in an unconscious manner, submerged relative to higher neural functions, 1 and a sense that has been increasingly reduced during the course of primate evolution. 1 - 8 Anatomical structures related to olfaction differ profoundly in proportions and complexity between higher taxonomic groups of primates (Haplorhini, Strepsirrhini). These anatomical differences are beyond dispute (Box 1). However, the relationship between the anatomical differences and primate sensory abilities, and hence the validity of using them to group primates into “microsmatic” or “macrosmatic” categories, 9 , 10 is less clear when we examine the physiological and genetic data on primate olfaction.     

The Ecology and Evolution of Fruit Odor: Implications for Primate Seed Dispersal

Primates are now known to possess a keen sense of smell that serves them in various contexts, including feeding. Many primate species are frugivorous and provide essential seed dispersal services to a variety of plants. Studies of pollination ecology, and recently seed dispersal ecology, indicate that animal mutualist behavior exerts selection pressures that drive changes in flower and fruit traits. As a result, the use of olfaction in in primate feeding ecology may have affected the evolution of fruit odor in species that rely on primate seed dispersal. However, this hypothesis is seldom tested. Here, we summarize the available information on how primates may have affected the evolution of fruit odor. We ask what the chemistry of primate fruit odor may look like, what information fruit odor may convey, whether there are geographical differences in fruit odor, and what other factors may affect the odor of fruits consumed by primates. We identify many gaps in the available data and offer research questions, hypotheses, and predictions for future studies. Finally, to facilitate standardization in the field, we discuss methodological issues in the process of odor sampling and analysis.     

The sense of smell: molecular basis of odorant recognition

Most animal species rely on odorant compounds to locate food, predators, or toxins. The sense of smell is also involved in animal communication, and revealing the underlying mechanisms will therefore facilitate a deeper understanding of animal behaviour. Since the 1940s different theories have speculated on the fundamental basis of olfaction. It was assumed that odorant molecules were recognized by selective protein receptors in the nose, triggering a nervous signal processed by the brain. The discovery of these receptors in the early 1990s allowed great progress in understanding the physiological and biochemical principles of olfaction. An overview of the different mechanisms involved in the coding of odour character as well as odour intensity is presented here, focusing on the biochemical basis of odorant recognition. Despite the enormous progress achieved in recent years, details of odorant-receptor interaction at the molecular level and the mechanisms of olfactory receptor activation are poorly understood. The likely role of metal ions in odorant recognition is discussed, and also the perireceptor events involved in odorant transport and biotransformation, with a view to providing a comprehensive overview of mammalian olfaction to guide future computational structural models and the design of functional experiments. Recent studies have analysed the olfactory genome of several species, providing information about the evolution of olfaction. The role of the olfactory system in animal communication is also described.     

Olfactory acuity in theropods: palaeobiological and evolutionary implications

This research presents the first quantitative evaluation of the olfactory acuity in extinct theropod dinosaurs. Olfactory ratios (i.e. the ratio of the greatest diameter of the olfactory bulb to the greatest diameter of the cerebral hemisphere) are analysed in order to infer the olfactory acuity and behavioural traits in theropods, as well as to identify phylogenetic trends in olfaction within Theropoda. A phylogenetically corrected regression of olfactory ratio to body mass reveals that, relative to predicted values, the olfactory bulbs of (i) tyrannosaurids and dromaeosaurids are significantly larger, (ii) ornithomimosaurs and oviraptorids are significantly smaller, and (iii) ceratosaurians, allosauroids, basal tyrannosauroids, troodontids and basal birds are within the 95% CI. Relative to other theropods, olfactory acuity was high in tyrannosaurids and dromaeosaurids and therefore olfaction would have played an important role in their ecology, possibly for activities in low-light conditions, locating food, or for navigation within large home ranges. Olfactory acuity was the lowest in ornithomimosaurs and oviraptorids, suggesting a reduced reliance on olfaction and perhaps an omnivorous diet in these theropods. Phylogenetic trends in olfaction among theropods reveal that olfactory acuity did not decrease in the ancestry of birds, as troodontids, dromaeosaurids and primitive birds possessed typical or high olfactory acuity. Thus, the sense of smell must have remained important in primitive birds and its presumed decrease associated with the increased importance of sight did not occur until later among more derived birds.     

Fruits, fingers, and fermentation: the sensory cues available to foraging primates

Survival and reproductive success hinge on the perception ofenvironmental stimuli. In this regard, foraging efficiency dependson discerning predictive signals in food. A widespread occurrenceof ethanol in fruits indicates a sustained historical exposureof frugivores to this compound. Accordingly, Dudley (2000, Quart.Rev. Biol. 75:3–15) proposed that ethanol could representa prominent sensory cue to primates because of direct and indirectlyassociated caloric and physiological rewards. However, littleis known regarding the extent to which ethanol correlates withsuch parameters. This information is essential to estimatingthe importance of detecting and detoxifying ethanol in fruits.Here I present a preliminary analysis of fruits from SoutheastAsia; low levels of ethanol were present in fruits of all developmentalstages (range: 0.005–0.48%). Moreover, ethanol correlatedpositively with concentrations of soluble sugars, suggestingthat it could be a valuable foraging cue. Recent findings onthe sensitivity of primate olfaction and gustation to ethanolare consistent with this notion. However, when primates smellfruits deliberately, it often occurs together with digital and/ordental evaluation of texture. Here I show that softening texturealso characterizes the fruit ripening process, and that coloris of ambiguous importance to primates possessing trichromaticvision. I discuss the relevance of these findings to the originsof primates and the ecology of key sensory systems and deducethat detecting and selecting fruits on the basis of cues otherthan color is a persistent theme in primate evolution. Ethanolhas likely played a significant and underestimated role in theregulation of primate foraging behavior.     

鸟类社会行为中的嗅觉通讯研究进展

长期以来, 学者普遍认为大多数鸟类的嗅觉能力较弱或丧失。早期实验未能得到统一而清晰的结果, 进一步扩大了这一认知误区。随着研究手段和技术的发展, 解剖学、电生理学、分子生物学和行为生态学等学科提供了鸟类嗅觉存在的证据。目前, 相关研究在鸟类14目33科中发现了嗅觉通讯的证据。与视觉和听觉一样, 这一感觉通路可能在鸟类的觅食、导航、防御、隐蔽、警戒和交流等社会行为中发挥着重要作用。本文着重于嗅觉通讯在鸟类社会行为中的功能, 通过回顾近十年的相关研究, 综述鸟类嗅觉在物种和个体识别、繁殖行为、亲缘识别、配偶选择与竞争等方面发挥的作用。我们也指出: 研究手段的创新将揭示更多鸟类物种在社会行为中对于嗅觉通讯的运用。此外, 当前研究多聚焦于少数物种和单一层面(如生理、生态和环境等), 使用分子生物学、解剖与生理学、行为学和神经生物学手段的整合研究较为缺乏; 而后者更有可能全面地揭示鸟类嗅觉通讯的复杂机理及其在社会行为中发挥的多种功能。     

Evolutionary changes of the importance of olfaction in cetaceans based on the olfactory marker protein gene

Odontocetes and mysticetes are two extant suborders of cetaceans. It is reported that the former have no sense of olfaction, while the latter can smell in air. To explain the ecological reason why mysticetes still retain their sense of smell, two hypotheses have been proposed — the echolocation-priority hypothesis, which assumes that the acquisition of echolocation causes the reduction of the importance of olfaction, and the filter-feeder hypothesis, which assumes that olfactory ability is important for filter-feeders to locate their prey because clouds of plankton give off a peculiar odor. The olfactory marker protein (OMP) is almost exclusively expressed in vertebrate olfactory receptor neurons, and is considered to play important roles in olfactory systems. In this study, full-length open reading frames of OMP genes were identified in 6 cetacean species and we analyzed the nonsynonymous to synonymous substitution rate ratio based on the maximum likelihood method. The evolutionary changes of the selective pressures on OMP genes did fit better to the filter-feeder hypothesis than to the echolocation-priority hypothesis. In addition, no pseudogenization mutations are found in all five odontocetes OMP genes investigated in this study. It may suggest that OMP retains some function even in ‘anosmic’ odontocetes.     

Human olfactory neurons respond to odor stimuli with an increase in cytoplasmic Ca2+.

The sense of smell allows terrestrial animals to collect information about the chemical nature of their environment through the detection of airborne molecules. In humans smell is believed to play an important role in protecting the organism from environmental hazards such as fire, gas leaks and spoiled food, in determining the flavor of foods, and perhaps in infant-parent bonding. In addition, the study of human olfaction is relevant to a number of medical problems that result in olfactory dysfunction, which can affect nutritional state, and to the study of the etiology of neurodegenerative diseases which manifest themselves in the olfactory epithelium. Although much is known about behavioral aspects of human olfaction, little is understood about the underlying cellular mechanisms in humans. Here we report that viable human olfactory neurons (HON) can be isolated from olfactory tissue biopsies, and we find that HON respond to odorants with an increase in intracellular calcium concentration ([Cai]).     

Morituri te salutant? Olfactory signal transduction and the role of phosphoinositides

During the past 150 years, researchers have investigated the cellular, physiological, and molecular mechanisms underlying the sense of smell. Based on these efforts, a conclusive model of olfactory signal transduction in the vertebrate's nose is now available, spanning from G-protein-mediated odorant receptors to ion channels, which are linked by a cyclic adenosine 3',5'-monophosphate-mediated signal transduction cascade. Here we review some historical milestones in the chronology of olfactory research, particularly emphasising the role of cyclic nucleotides and inositol trisphosphate as alternative second messengers in olfactory cells. We will describe the functional anatomy of the nose, outline the cellular composition of the olfactory epithelium, and describe the discovery of the molecular backbone of the olfactory signal transduction cascade. We then summarize our current model, in which cyclic adenosine monophosphate is the sole excitatory second messenger in olfactory sensory neurons. Finally, a possible significance of microvillous olfactory epithelial cells and inositol trisphosphate in olfaction will be discussed.     

Primates got personality,too: Toward an integrative primatology of consistent individual differences in behavior

In recent years, research on animal personality has exploded within the field of behavioral ecology. Consistent individual differences in behavior exist in a wide range of species, and these differences can have fitness consequences and influence several aspects of a species' ecology. In comparison to studies of other animals, however, there has been relatively little research on the behavioral ecology of primate personality. This is surprising given the large body of research within psychology and biomedicine showing that primate personality traits are heritable and linked to health and life history outcomes. In this article, I bring together theoretical perspectives on the ecology and evolution of animal personality with an integrative review of what we know about primate personality from studies conducted on captive, free‐ranging, and wild primates. Incorporating frameworks that emphasize consistency in behavior into primate behavioral ecology research holds promise for improving our understanding of primate behavioral evolution.     

Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates

Olfactory receptor (OR) genes constitute the molecular basis for the sense of smell and are encoded by the largest gene family in mammalian genomes. Previous studies suggested that the proportion of pseudogenes in the OR gene family is significantly larger in humans than in other apes and significantly larger in apes than in the mouse. To investigate the process of degeneration of the olfactory repertoire in primates, we estimated the proportion of OR pseudogenes in 19 primate species by surveying randomly chosen subsets of 100 OR genes from each species. We find that apes, Old World monkeys and one New World monkey, the howler monkey, have a significantly higher proportion of OR pseudogenes than do other New World monkeys or the lemur (a prosimian). Strikingly, the howler monkey is also the only New World monkey to possess full trichromatic vision, along with Old World monkeys and apes. Our findings suggest that the deterioration of the olfactory repertoire occurred concomitant with the acquisition of full trichromatic color vision in primates.     

Pheromones in birds: myth or reality?

Birds are anosmic or at best microsmatic… This misbelief persisted until very recently and has strongly influenced the outcome of communication studies in birds, with olfaction remaining neglected as compared to acoustic and visual channels. However, there is now clear empirical evidence showing that olfaction is perfectly functional in birds and birds use olfactory information in a variety of ethological contexts. Although the existence of pheromones has never been formally demonstrated in this vertebrate class, different groups of birds, such as petrels, auklets and ducks have been shown to produce specific scents that could play a significant role in within-species social interactions. Behavioral experiments have indeed demonstrated that these odors influence the behavior of conspecifics. Additionally, in quail, deprivation of olfactory inputs decreases neuronal activation induced by sexual interactions with a female. It seems therefore well established that birds enjoy a functional sense of smell and a fast growing body of experimental evidence suggests that they use this channel of olfactory communication to control their social life. The unequivocal identification of an avian pheromone is, however, still ahead of us but there are now many exciting opportunities to unravel the behavioral and physiological particularities of chemical communication in birds.     

The neglected sense-olfaction in primate behavior, ecology, and evolution

This special issue emerged from a symposium held during the 20th Congress of the International Primatological Society in Torino, Italy, in August 2004. The symposium brought together scientists studying several different aspects of olfaction in primates. The topics addressed ranged from the morphology and physiology of the sensory apparatus, the genetics and chemistry of olfactory signals and the use of such signals in primate communication, to a comparative analysis of the role of olfaction in neural evolution. The papers in this issue reflect a surge of interest in diverse aspects of olfaction-an interest that has been stimulated by the more rigorous theoretical approaches and new techniques that have recently become available. This introduction briefly reviews past research on primate olfaction, summarizes the scope of this special issue, and provides a somewhat speculative glimpse of the future.     

Learning about the functions of the olfactory system from people without a sense of smell

The olfactory system provides numerous functions to humans, influencing ingestive behavior, awareness of environmental hazards and social communication. Approximately ⅕ of the general population exhibit an impaired sense of smell. However, in contrast to the many affected, only few patients complain of their impairment. So how important is it for humans to have an intact sense of smell? Or is it even dispensable, at least in the Western world? To investigate this, we compared 32 patients, who were born without a sense of smell (isolated congenital anosmia - ICA) with 36 age-matched controls. A broad questionnaire was used, containing domains relevant to olfaction in daily life, along with a questionnaire about social relationships and the BDI-questionnaire. ICA-patients differed only slightly from controls in functions of daily life related to olfaction. These differences included enhanced social insecurity, increased risk for depressive symptoms and increased risk for household accidents. In these domains the sense of olfaction seems to play a key role.     

Modeling Olfactory Bulb Evolution through Primate Phylogeny

Adaptive characterizations of primates have usually included a reduction in olfactory sensitivity. However, this inference of derivation and directionality assumes an ancestral state of olfaction, usually by comparison to a group of extant non-primate mammals. Thus, the accuracy of the inference depends on the assumed ancestral state. Here I present a phylogenetic model of continuous trait evolution that reconstructs olfactory bulb volumes for ancestral nodes of primates and mammal outgroups. Parent-daughter comparisons suggest that, relative to the ancestral euarchontan, the crown-primate node is plesiomorphic and that derived reduction in olfactory sensitivity is an attribute of the haplorhine lineage. The model also suggests a derived increase in olfactory sensitivity at the strepsirrhine node. This oppositional diversification of the strepsirrhine and haplorhine lineages from an intermediate and non-derived ancestor is inconsistent with a characterization of graded reduction through primate evolution.     

Evidence for increased olfactory receptor gene repertoire size in two nocturnal bird species with well-developed olfactory ability

Background  

In vertebrates, the molecular basis of the sense of smell is encoded by members of a large gene family, namely olfactory receptor (OR) genes. Both the total number of OR genes and the proportion of intact OR genes in a genome may indicate the importance of the sense of smell for an animal. There is behavioral, physiological, and anatomical evidence that some bird species, in particular nocturnal birds, have a well developed sense of smell. Therefore, we hypothesized that nocturnal birds with good olfactory abilities have evolved (i) more OR genes and (ii) more intact OR genes than closely related and presumably less 'olfaction-dependent' day-active avian taxa.     

Conserved, highly specialized olfactory receptor neurons for food compounds in 2 congeneric scarab beetles, Pachnoda interrupta and Pachnoda marginata

Few studies have systematically addressed evolutionary changes in olfactory neuron assemblies, either by genetic drift or as an adaptation to specific odor environments. We have studied the sense of olfaction in 2 congeneric scarab beetles, Pachnoda interrupta Olivier and Pachnoda marginata Drury (Coleoptera: Scarabaeidae: Cetoniinae), which are both opportunistic polyphages, feeding mainly on fruit and flowers. The 2 species occur in dissimilar habitats: P. interrupta is found in dry savannah, and P. marginata in tropical parts of equatorial Africa. To study how these species may have adapted their sense of olfaction to their odor environments, we utilized single-unit electrophysiology on olfactory sensilla with a wide selection of food-related compounds. Despite the differences in habitat, we found that the species shared most of the physiological types of olfactory receptor neurons (ORNs) encountered, although their proportions frequently varied between the species. The high degree of conservation in olfaction between the species implies that a similar sensory strategy is efficient for food search in both habitats. However, shifts in proportions of receptor neuron classes, and slight shifts in response profiles and/or presence of some ORN classes unique to either species, may reflect adaptation to a different set of hosts.     

How Far Does a Receptor Influence Vibrational Properties of an Odorant?

The biophysical mechanism of the sense of smell, or olfaction, is still highly debated. The mainstream explanation argues for a shape-based recognition of odorant molecules by olfactory receptors, while recent investigations suggest the primary olfactory event to be triggered by a vibrationally-assisted electron transfer reaction. We consider this controversy by studying the influence of a receptor on the vibrational properties of an odorant in atomistic details as the coupling between electronic degrees of freedom of the receptor and the vibrations of the odorant is the key parameter of the vibrationally-assisted electron transfer. Through molecular dynamics simulations we elucidate the binding specificity of a receptor towards acetophenone odorant. The vibrational properties of acetophenone inside the receptor are then studied by the polarizable embedding density functional theory approach, allowing to quantify protein-odorant interactions. Finally, we judge whether the effects of the protein provide any indications towards the existing theories of olfaction.     

Physiological Ecology of Howlers (Alouatta): Energetic and Digestive Considerations and Comparison with the Colobinae

Remarkably little attention has been focused on the physiological ecology of free-ranging primates. Yet without such information, it may prove difficult to advance our understanding of factors influencing the dietary behavior of wild primates much beyond its present state. Mantled howlers (Alouatta palliata) have been studied in terms of some features of physiological ecology. Results of this work have helped to clarify some factors influencing howler and other primate food choices in the natural environment and have called into question various assumptions about leaf-eating primates. For example, though howlers eat considerable foliage, they do not exhibit a lower than predicted basal metabolic rate, nor do available data suggest that secondary compounds strongly influence howler food selection. Comparison of howlers with members of the Colobinae reveals some differences in features of their respective energetic and digestive physiology and raises timely issues for future research.