Structure and function of the vomeronasal system: an update

We report the sequencing at 131× coverage, de novo assembly and analyses of the genome of a female Tibetan wild boar. We also resequenced the whole genomes of 30 Tibetan wild boars from six major distributed locations and 18 geographically related pigs in China. We characterized genetic diversity, population structure and patterns of evolution. We searched for genomic regions under selection, which includes genes that are involved in hypoxia, olfaction, energy metabolism and drug response. Comparing the genome of Tibetan wild boar with those of neighboring Chinese domestic pigs further showed the impact of thousands of years of artificial selection and different signatures of selection in wild boar and domestic pig. We also report genetic adaptations in Tibetan wild boar that are associated with high altitudes and characterize the genetic basis of increased salivation in domestic pig.

Genomic analyses identify distinct patterns of selection in domesticated pigs and Tibetan wild boars

Mammalian social systems rely on signals passed between individuals conveying information including sex, reproductive status, individual identity, ownership, competitive ability and health status. Many of these signals take the form of complex mixtures of molecules sensed by chemosensory systems and have important influences on a variety of behaviours that are vital for reproductive success, such as parent-offspring attachment, mate choice and territorial marking. This article aims to review the nature of these chemosensory cues and the neural pathways mediating their physiological and behavioural effects. Despite the complexities of mammalian societies, there are instances where single molecules can act as classical pheromones attracting interest and approach behaviour. Chemosignals with relatively high volatility can be used to signal at a distance and are sensed by the main olfactory system. Most mammals also possess a vomeronasal system, which is specialized to detect relatively non-volatile chemosensory cues following direct contact. Single attractant molecules are sensed by highly specific receptors using a labelled line pathway. These act alongside more complex mixtures of signals that are required to signal individual identity. There are multiple sources of such individuality chemosignals, based on the highly polymorphic genes of the major histocompatibility complex (MHC) or lipocalins such as the mouse major urinary proteins. The individual profile of volatile components that make up an individual odour signature can be sensed by the main olfactory system, as the pattern of activity across an array of broadly tuned receptor types. In addition, the vomeronasal system can respond highly selectively to non-volatile peptide ligands associated with the MHC, acting at the V2r class of vomeronasal receptor. The ability to recognize individuals or their genetic relatedness plays an important role in mammalian social behaviour. Thus robust systems for olfactory learning and recognition of chemosensory individuality have evolved, often associated with major life events, such as mating, parturition or neonatal development. These forms of learning share common features, such as increased noradrenaline evoked by somatosensory stimulation, which results in neural changes at the level of the olfactory bulb. In the main olfactory bulb, these changes are likely to refine the pattern of activity in response to the learned odour, enhancing its discrimination from those of similar odours. In the accessory olfactory bulb, memory formation is hypothesized to involve a selective inhibition, which disrupts the transmission of the learned chemosignal from the mating male. Information from the main olfactory and vomeronasal systems is integrated at the level of the corticomedial amygdala, which forms the most important pathway by which social odours mediate their behavioural and physiological effects. Recent evidence suggests that this region may also play an important role in the learning and recognition of social chemosignals.

/pdf/mammalian-social-odours-attraction-and-individual-1e2ymdm9h9.pdf

Mammalian social odours: attraction and individual recognition

In the 1960s, when population geneticists first began to collect data on the amount of genetic variation in natural populations, balancing selection was invoked as a possible explanation for how such high levels of molecular variation are maintained. However, the predictions of the neutral theory of molecular evolution have since become the standard by which cases of balancing selection may be inferred. Here we review the evidence for balancing selection acting on the major histocompatibility complex (MHC) of vertebrates, a genetic system that defies many of the predictions of neutrality. We apply many widely used tests of neutrality to MHC data as a benchmark for assessing the power of these tests. These tests can be categorized as detecting selection in the current generation, over the history of populations, or over the histories of species. We find that selection is not detectable in MHC datasets in every generation, population, or every evolutionary lineage. This suggests either that selection on the MHC is heterogeneous or that many of the current neutrality tests lack sufficient power to detect the selection consistently. Additionally, we identify a potential inference problem associated with several tests of neutrality. We demonstrate that the signals of selection may be generated in a relatively short period of microevolutionary time, yet these signals may take exceptionally long periods of time to be erased in the absence of selection. This is especially true for the neutrality test based on the ratio of nonsynonymous to synonymous substitutions. Inference of the nature of the selection events that create such signals should be approached with caution. However, a combination of tests on different time scales may overcome such problems.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.0014-3820.2003.tb00580.x

Perspective: detecting adaptive molecular polymorphism: lessons from the MHC.

What produces emotions? Why and how do we have emotions? Why do emotional states feel like something? What is the relation between emotion, and reward value, and subjective feelings of pleasure? How does the brain implement decision-making? Are gene-defined rewards and emotions in the interests of the genes, and does rational multistep planning enable us to go beyond selfish genes to long-term plans and social contracts in the interests of the individual? This book seeks explanations of emotion and decision-making by considering these and other questions

Emotion and decision making explained

The major histocompatibility complex (MHC) is a source of unique individual odors that influence individual recognition, mating preferences, nesting behavior and selective block of pregnancy in animals. Such phenomena have been difficult to study in humans, because the human leukocyte antigen (HLA, human MHC) loci are the most polymorphic loci in the human genome, with the potential to generate millions of unique combinations of genotypes. In addition, high variability in background odors, encoded by the rest of the genome and influenced by cultural practices, contribute to a low signal-to-noise ratio that could mask HLA-based olfactory cues. Here we show that women can detect differences of one HLA allele among male odor donors with different MHC genotypes. Notably, the mechanism for a woman's ability to discriminate and choose odors is based on HLA alleles inherited from her father but not her mother. The parents' HLA alleles that she does not inherit show no relationship with odor choice, despite exposure to these HLA-encoded odors throughout her life. Our data indicate that paternally inherited HLA-associated odors influence odor preference and may serve as social cues.

Paternally inherited HLA alleles are associated with women's choice of male odor.

Objective: To characterize the nasal opening of the human nasopalatine duct (NPD; a major duct of the vomeronasal system used in animals for chemical communication) by identifying its location, categorizing variations in physical characteristics, and assessing frequency of detection. Design: Two studies: (1) general study incorporating endoscopic examinations documented by videotapes and photographs, and an investigation of detection bias in terms of method of visualization and defining criteria for NPD identification; and (2) cadaver dissections examining NPD gross anatomy and proximity to the putative vomeronasal organ (VNO), the second major duct of the vomeronasal system.

https://jamanetwork.com/journals/jamaotolaryngology/articlepdf/404862/ooa90148.pdf

Location and gross morphology of the nasopalatine duct in human adults.

Males of certain species of fairy-wrens (Aves: Maluridae) emit a unique vocalization, the Type II vocalization, in response to the calls of potential predators. We conducted field observations and playback experiments to identify the contexts in which the Type II vocalization is emitted by splendid fairy-wren (Malurus splendens) males, and to examine social and genetic factors that influence its occurrence. In field observations and controlled playback experiments, Type II vocalizations were elicited most consistently by calls of the predatory gray butcherbird (Cracticus torquatus). Some vocalizations from other avian species also elicited Type II vocalizations, and the majority of these were vocalizations from avian predators. Splendid fairy-wrens are cooperative breeders, and males that responded with Type II vocalizations to playbacks of butcherbird calls tended to be primary rather than secondary males, had larger cloacal protuberances, and were older than those that did not respond. In addition, secondary males that were sons of resident females were more likely than non-sons to respond with a Type II vocalization. In another playback experiment, females responded similarly to the Type I song and Type II vocalizations of their mates. Although the Type II vocalization is emitted primarily in response to predator calls, it is inconsistent with an alarm call explanation. Patterns of reproductive success among Type II calling males suggest that it does not function as an honest signal of male quality. At present, the function of the vocalization remains anomalous, but indirect fitness benefits may play a role in its explanation.

Singing in the Face of Danger: the Anomalous Type II Vocalization of the Splendid Fairy-Wren

Pheromones and vasanas: the functions of social chemosignals.

Jacob et al.1 published in February’s issue of Nature Genetics differ from those of most previous studies of the major histocompatibility complex (MHC) and mate or odor preference in any animal2. It is therefore important to understand what may have caused these differences. In this study1, 49 smellers (who were handled as independent replicates in the statistical analysis) chose the most and the least preferred odor out of only six body odors provided by donors of different ethnic background. This is a kind of pseudoreplication3,4 that can easily create misleading results. If, for example, only one donor with rather rare MHC alleles tended to smell slightly less pleasant than others because of something that is not correlated to the MHC (such as odor intensity5 or an illness), this would produce a bias in the analysis towards the conclusion that MHC-similar types smelled better. Such arbitrary shifts of mean pleasantness can cause all sorts of incorrect results (Fig. 1). By contrast, an analysis based on withindonor comparisons5,6 would not be changed by such constant shifts of pleasantness scores. These arbitrary effects depend on the number of allele matches between each donor and the smellers. In an outbred group of non-kin (such as a typical sample of college students5,6), identical haplotypes are rare and donors are not expected to differ, on average, in the number of allele matches to the maternally and the paternally inherited genotypes of the smellers. The smellers in the study by Jacob et al.1 were members of an inbred group that has only a few haplotypes. This increases the risk that, in a given sample, MHC alleles will not be equally distributed to maternally and paternally inherited genotypes. Indeed, the MHC alleles in this case happened to be distributed non-randomly (Fig. 2). This fact, combined with the aforementioned arbitrary effects, can cause all sorts of outcomes that only appear to be caused differentially by maternal and paternal MHC types. Therefore, the conclusions that women have paternally inherited odor preferences1 and that they prefer odors of MHC-similar donors1 are not justified.

The MHC and body odors: arbitrary effects caused by shifts of mean pleasantness. Authors' reply

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