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Penn DJ, Potts WK. How do major histocompatibility complex genes influence odor and mating preference? Adv Immunol 69: 411-436
... Existují důkazy, že pach u lidí i dalších druhů je ovlivněn vysoce polymorfním hlavním histokompatibilním komplexem (MHC, z angl. Major Histocompatibility Complex) [44][45][46][47]. U člověka je hlavním histokompatibilním systémem komplex HLA (z angl. ...
... Několik studií ukázalo, že hraje rozhodující roli v čichovém rozpoznávání sebe sama či příbuzných, stejně jako v chování v reprodukci u myší a jiných savců [48]. Některé studie dokonce naznačují, že může hrát roli v subjektivní přitažlivosti lidského pachu a ovlivnit tak výběr partnera [45,49,50]. Geny MHC jsou totožné pro monozygotní dvojčata, nemusí však být identické pro dvojčata dizygotní. ...
... Jednovaječná (monozygotní) dvojčata žijící v různých prostředích pak mohou sdílet stejný primární pach, ne však nutně pach sekundární. [4] Vliv MHC může být popsán čtyřmi různými hypotézami [45]: ...
Předkládaná dizertační práce je zaměřena na studium molekulárního profilu lidského kožního pachu pomocí metod plynové chromatografie ve spojení s hmotnostní detekcí (GC-MS a GC×GC-MS). V rámci této práce je představeno několik dílčích experimentů, zabývajících se optimální přípravou pachových vzorků pro chemickou analýzu (nalezení vhodných sorpčních materiálů, vhodných rozpouštědel pro následnou extrakci pachových sloučenin, způsobu koncentrování vzorků, či testování pachů z různých částí těla). Několik experimentů se pak věnuje možnostem provedení skupinové identifikace (konkrétně diskriminaci pohlaví) ze vzorků lidského pachu, a to za použití různých způsobů provedení analýzy. Poslední popisovaný a nejrozsáhlejší experiment (504 vzorků lidského pachu od 40 dobrovolníků, v nichž bylo sledováno 67 látek) se pak zabývá nejen skupinovou identifikací, ale i identifikací individuální. Za pomoci matematické metody podpůrných vektorů byly vytvořeny modely s přesností určení pohlaví kolem 90 %, klasifikační modely pro určení jednotlivce pak dosahovaly přesnosti kolem 70 %.
Dosažené výsledky ukazují, že detailní analýza molekulárního profilu pachu jedince umožňuje jak skupinovou, tak individuální identifikaci člověka, nicméně pro budoucí použitelnost ve forenzní praxi je třeba provést další experimenty, s cílem vybudovat rozsáhlou mezinárodní databázi pachových vzorků odebraných, připravených a zanalyzovaných unifikovaným způsobem tak, aby byly pachové vzorky porovnatelné a umožňovaly vytvoření přesných (více jak 95%) klasifikačních modelů.
... Because immune responses are mounted against microbial peptides matching the PBS of the MHC molecule, MHC allele diversity might determine the repertoire of peptide ligands that is available to the microbial community to metabolize. Furthermore, by immunologically controlling microbiota composition, MHC allele diversity might govern molecules and microbial secondary metabolites available to the microbes, the products of which might affect odor (Penn and Potts 1998a). Alternatively, regulation by the MHC might cause interspecific interactions between microbes and thus indirectly determine microbiota composition by favoring or preventing the establishment of certain species. ...
... The underlying chemical properties of the molecules suspected to carry information via direct or indirect mechanisms of MHC-linked odor signaling differ substantially (see Penn and Potts 1998a;Ruff et al. 2012;and Overath et al. 2014 for critical discussion of the mechanisms). Both the peptides bound by MHC molecules as well as the MHC molecules themselves, which are supposed to serve as odorants, are nonvolatile peptides. ...
... (6) Theories suggest that either MHC molecules themselves, the volatiles the MHC molecules might carry or volatiles developing due to the MHC's role in binding peptides could be potential sources of odor (Penn and Potts 1998a). However, what chemical components apart from MHC peptide ligands can enable or contribute to the discriminability of MHC-based odors has not yet been clearly determined. ...
Genes of the major histocompatibility complex (MHC) have long been linked to odor signaling and recently researchers’ attention has focused on MHC structuring of microbial communities and how this may in turn impact odor. However, understanding of the mechanisms through which the MHC could affect the microbiota to produce a chemical signal that is both reliable and strong enough to ensure unambiguous transmission of behaviorally important information remains poor. This is largely because empirical studies are rare, predictions are unclear, and the underlying immunological mechanisms governing MHC–microbiota interactions are often neglected. Here, we review the immunological processes involving MHC class II (MHC-II) that could affect the commensal community. Focusing on immunological and medical research, we provide background knowledge for nonimmunologists by describing key players within the vertebrate immune system relating to MHC-II molecules (which present extracellular-derived peptides, and thus interact with extracellular commensal microbes). We then systematically review the literature investigating MHC–odor–microbiota interactions in animals and identify areas for future research. These insights will help to design studies that are able to explore the role of MHC-II and the microbiota in the behavior of wild populations in their natural environment and consequently propel this research area forward.
... These symbiotic microbial networks have been primarily characterized in humans and other animals in controlled settings, but the relationship between microorganisms and wild animals, particularly in nonmammalian species, remains vastly understudied [3]. Understanding this "second genome" of wild animals is a critical step toward unraveling host-microbe co-evolutionary relationships [4], developmental and genomic interactions [5], and animal behaviors, including mating, predation, and self-recognition [6][7][8]. Better understanding of these processes using microbially informed approaches will aid in wildlife management, pathogen prevention, and wildlife veterinary practices. To date, the majority of wild animal microbiome studies focus on terrestrial mammals [7][8][9] and, comparatively, little is known about avian species [10], which account for over 15% of all vertebrates [11]. ...
... LESPs are known to use odor cues for several important behaviors, including predation, burrow relocation, and identification of conspecifics [36][37][38][39][40]. Because of the importance of olfaction in this species, it is an excellent model for examining microbial differences between individuals, which may relate to volatile organic compound production on the skin [6]. On Bon Portage Island, located off the southern tip of the Canadian province of Nova Scotia in North America, LESPs are abundant, accessible and easily handled, which allows for larger sample sizes than would be possible with other types of olfactory seabirds [41]. ...
... The MHC is a class of highly polymorphic immunogenetic markers, whose variability in natural populations is maintained by pathogen-mediated selection, disassortative mate choice, and maternal-fetal effects [25]. In some organisms, MHC appears to influence individual body odor, possibly due to interactions with microbial communities [6]. For example, in black-legged kittawakes, chemicals found in preen secretions correlate positively with MHC relatedness [102]. ...
Background
The microbiome provides multiple benefits to animal hosts that can profoundly impact health and behavior. Microbiomes are well-characterized in humans and other animals in controlled settings, yet assessments of wild bird microbial communities remain vastly understudied. This is particularly true for pelagic seabirds with unique life histories that differ from terrestrial bird species. This study was designed to examine how morphological, genetic, environmental, and social factors affect the microbiome of a burrow-nesting seabird species, Leach’s storm petrel (Oceanodroma leucorhoa). These seabirds are highly olfactory and may rely on microbiome-mediated odor cues during mate selection. Composition and structure of bacterial communities associated with the uropygial gland and brood patch were assessed using 16S rRNA amplicon-based Illumina Mi-Seq analysis and compared to burrow-associated bacterial communities. This is the first study to examine microbial diversity associated with multiple body sites on a seabird species.
Results
Results indicate that sex and skin site contribute most to bacterial community variation in Leach’s storm petrels and that major histocompatibility complex (MHC) genotype may impact the composition of bacterial assemblages in males. In contrast to terrestrial birds and other animals, environmental and social interactions do not significantly influence storm petrel-associated bacterial assemblages. Thus, individual morphological and genetic influences outweighed environmental and social factors on microbiome composition.
Conclusions
Contrary to observations of terrestrial birds, microbiomes of Leach’s storm petrels vary most by the sex of the bird and by the body site sampled, rather than environmental surroundings or social behavior.
Electronic supplementary material
The online version of this article (10.1186/s40168-017-0365-4) contains supplementary material, which is available to authorized users.
... Third, another laboratory experiment with MHC-congenic mice found that cross-fostering altered the mating (first mount) preferences of one of two strains of female mice tested compared with unfostered mice (Eklund 1997a). Finally, we recently found that cross-fostering reverses the MHC-disassortative mating preferences of wild-derived female mice living in seminatural conditions (Penn and Potts 1998c). Taken together, these cross- fostering studies provide strong experimental evidence for MHC-dependent mating preferences and familial imprinting. ...
... The selection from mating preferences was sufficient to maintain the diversity of MHC genes found in wild pop- ulations (Hedrick 1992). Furthermore, we recently found that the MHC-disassortative mating preferences of female mice living in seminatural enclosures can be reversed by cross-fostering ( Penn and Potts 1998c). This supports lab- oratory studies showing familial imprinting in inbred, lab- oratory strains of mice ( Beauchamp et al. 1988;Yamazaki et al. 1988; Eklund 1997a), as well as the original finding of MHC-dependent mating preferences in wild-derived mice ( Potts et al. 1991). ...
... Fourth, MHC-heterozygote advantage may be over- looked if the benefit of heterozygosity lies in reduced im- munopathology rather then increased immune respon- siveness (Carter et al. 1992). Immune responses can be too strong as well as too weak; however, experimental studies have generally ignored immunopathology even though it is probably the most important cost of immu- nological defenses (Wakelin 1997;Gemmill and Read 1998;Penn and Potts 1998d). One problem with this "optimal immunity" hypothesis is that experimental evidence from mice indicates that MHC heterozygotes respond more ag- gressively to infection and consequently suffer more im- munopathology than homozygotes (Doherty and Zinkernagel 1975). ...
House mice prefer mates genetically dissimilar at the major histocompatibility complex (MHC). The highly polymorphic MHC genes control immunological self/nonself recognition; therefore, this mating preference may function to provide “good genes” for an individual's offspring. However, the evidence for MHC‐dependent mating preferences is controversial, and its function remains unclear. Here we provide a critical review of the studies on MHC‐dependent mating preferences in mice, sheep, and humans and the possible functions of this behavior. There are three adaptive hypotheses for MHC‐dependent mating preferences. First, MHC‐disassortative mating preferences produce MHC‐heterozygous offspring that may have enhanced immunocompetence. Although this hypothesis is not supported by tests of single parasites, MHC heterozygotes may be resistant to multiple parasites. Second, we propose that MHC‐dependent mating preferences enable hosts to provide a “moving target” against rapidly evolving parasites that escape immune recognition (the Red Queen hypothesis). Such parasites are suspected to drive MHC diversity through rare‐allele advantage. Thus, the two forms of parasite‐mediated selection thought to drive MHC diversity, heterozygote and rare‐allele advantage, will also favor MHC‐dependent mating preferences. Finally, MHC‐dependent mating preferences may also function to avoid inbreeding; a hypothesis consistent with other evidence that MHC genes play a role in kin recognition.
... Our experimentally obtained results on house sparrows do not provide evidence of MHC-I scent discrimination in a passerine bird species. Although olfaction has been shown to play a major role in assessing genetic dissimilarity in birds [28,29] as well as in other taxa [62], our results show that neither females nor males exhibited any preference for the scent of conspecifics with greater MHC-I diversity or dissimilarity. This is contrary to previous studies showing [28], and female song sparrow (Melospiza melodia) preferred the scent of MHC-II-dissimilar and more MHC-II-diverse males during the mating period [29]. ...
... Collectively, the contradictory results of our study and others suggest that more research is needed to examine the mechanisms in more detail that may account for the olfactory assessment of MHC-I characteristics in birds. Although, several hypotheses have been proposed to explain the underlying mechanisms [62], it is still not completely understood how MHC genes influence scent [69,70]. As MHC proteins appear in urine and sweat, it was proposed that these molecules may constitute odorants [71]. ...
MHC genes play a fundamental role in immune recognition of pathogens and parasites. Therefore, females may increase offspring heterozygosity and genetic diversity by selecting males with genetically compatible or heterozygous MHC. In birds, several studies suggest that MHC genes play a role in mate choice, and recent evidence suggests that olfaction may play a role in the MHC-II discrimination. However, whether olfaction is involved in MHC-I discrimination in birds remains unknown. Previous studies indicate that house sparrow females with low allelic diversity prefer males with higher diversity in MHC-I alleles. Here, we directly explored whether female and male house sparrows ( Passer domesticus ) could estimate by scent MHC-I diversity and/or dissimilarity of potential partners. Our results show that neither females nor males exhibit a preference related to MHC-I diversity or dissimilarity of potential partners, suggesting that MHC-I is not detected through olfaction. Further studies are needed to understand the mechanisms responsible for mate discrimination based on MHC-I in birds.
... One sensory modality that transports the information about an individual's MHC was revealed again in mice: odor. The choice between urine odor from MHC similar and dissimilar mice in a y-maze favored MHC dissimilar individuals e.g., [5,[47][48][49][50][51][52][53][54]. Thus, odor transmits the MHC signal and the choosing mouse knows her own MHC otherwise she could not prefer 'dissimilar'. ...
... "The problem with the carrier hypothesis is that it is difficult to imagine how binding properties of MHC molecules might be converted from being hydrophilic peptides-binding molecules to hydrophobic aromatic-binding molecules" [52]. Even if one would agree with the "empty platform" being able to bind a cocktail of volatiles, how could the released molecules of the 'cocktail' transport the information content of the specific sequence of amino acids mirroring the binding cleft of the MHC molecule? ...
Although an individual’s mix of MHC immune genes determines its resistance, finding MHC-dependent mate choice occurred by accident in inbred mice. Inbred mice prefer MHC dissimilar mates, even when the choice was restricted to urine. It took decades to find the info-chemicals, which have to be as polymorphic as the MHC. Microbiota were suggested repeatedly as the origin of the odor signal though germ-free mice maintained normal preference. Different versions of the ‘carrier hypothesis’ suggested MHC molecules carry volatiles after the bound peptide is released. Theory predicted an optimal individual MHC diversity to maximize resistance. The optimally complementary mate should be and is preferred as several studies show. Thus, the odor signal needs to transmit the exact information of the sender’s MHC alleles, as do MHC ligand peptides but not microbiota. The ‘MHC peptide hypothesis’ assumes that olfactory perception of the peptide ligand provides information about the MHC protein in a key-lock fashion. Olfactory neurons react only to the anchors of synthesized MHC peptides, which reflect the binding MHC molecule’s identity. Synthesized peptides supplemented to a male’s signal affect choice in the predicted way, however, not when anchors are mutated. Also, the human brain detects smelled synthesized self-peptides as such. After mate choice, the lottery of meiosis of randomly paired oocyte and sperm haplotypes would often produce MHC non-optimal offspring. In sticklebacks, eggs select MHC-compatible sperm, thus prefer the best combination close to the population optimum.
... Mice can discriminate odors from other mice that differ in only a single MHC haplotype (Penn and Potts, 1998a). Mice can also discriminate between two MHC haplotypes differing only in their peptide-binding site (Carroll et al., 2002). ...
... Other MHC-regulated behaviors include kin recognition and pregnancy blockage after a changeover in dominant males (Slev et al., 2006). Specific olfactory cues associated with the MHC and its genetic background can also be identified by rats (Eggert et al., 1996;Penn and Potts, 1998a). MHC class I peptides in urine clearly influence mouse behaviors. ...
Odors may be pleasant or unpleasant and in practice, pleasant odors are attractive while unpleasant odors are repellent. However, an odor that is noxious to one species may be attractive to another. Plants, predators, and pathogens may enhance their transmission by manipulating these signals. This may be especially significant when odors attract arthropod disease vectors. Odor detection may also be important in small prey species for evasion of macropredators such as large carnivores. Conversely, pleasant odors may identify family members, parents, or sexual partners. They may also generate signals of good health or fitness and contribute to the process of mate selection. In this review, we seek to integrate these odor-driven processes into a coherent pattern of behaviors that serve to complement the innate and adaptive immune systems. It may be considered the ‘behavioral immune system’.
... In yellowthroats (Geothlypis trichas), MHC diversity is correlated with facial mask size or bib brightness (Dunn, Bollmer, Freeman-Gallant, & Whittingham, 2013;Whittingham, Freeman-Gallant, Taff, & Dunn, 2015). Mice prefer mates with dissimilar MHC genotypes, which they detect through the impacts of these genes on body odour (Penn & Potts, 1998). In three-spined sticklebacks (Gasterosteus aculeatus), male breeding coloration is most intense in individuals with maximal MHC class I diversity (Jäger et al., 2007). ...
... Vertebrates advertise "good genes" through different kinds of cues (Johansson & Jones, 2010;Ziegler, Kentenich, & Uchanska-Ziegler, 2005 (Singer, Beauchamp, & Yamazaki, 1997) or changing intestinal flora (Penn & Potts, 1998), making body odour a source of MHC information. Birds do not typically have an acute sense of smell (Jones & Roper, 1997), but they do possess highly developed vision (Eaton, 2005). ...
1.Although vertebrates have been reported to gain higher reproductive outputs by choosing mates, few studies have been conducted on threatened species. However, species recovery should benefit if natural mate choice could improve reproductive output (i.e., pair performance related to offspring number, such as increased clutch size, numbers of fertilized egg and fledglings). We assessed the evidence for major histocompatibility complex (MHC)‐based mate preference in the endangered crested ibis (Nipponia nippon), and quantified the impacts of such choice on reproductive output. 2. We tested the hypothesis that crested ibis advertise “good genes” through external traits, by testing whether nuptial plumage characteristics and body morphology mediate mate choice for underlying genetic MHC variation. 3. We found differences between males and females in preferred MHC genotypes, external traits used in mate choice, and contributions to reproductive outputs. Females preferred MHC‐heterozygous males, which had darker [i.e., lower total reflectance and ultraviolet (UV) reflectance] nuptial plumage. Males preferred females lacking the DAB*d allele at the MHC classIIDAB locus, which had higher average body mass. DAB*d‐free females yielded heavier eggs and more fledglings, while MHC‐heterozygous males contributed to more fertilized eggs and fledglings. Fledging rate was highest when both parents had the preferred MHC genotypes (i.e., MHC‐heterozygous father and DAB*d‐free mother). Comparisons showed that free‐mating wild and seminatural pairs yielded more fertilized eggs and more fledglings, with a higher fledging rate, than captive pairs matched artificially based on pedigree. 4. Conservation programs seldom apply modern research results to population management, which could hinder recovery of threatened species. Our results show that mate choice can play an important role in improving reproductive output, with an example in which an endangered bird selects mates using UV visual capability. Despite the undoubted importance of pedigree‐based matching of mates in conservation programs, we show that free‐mating can be a better alternative strategy. This article is protected by copyright. All rights reserved.
... species level [18,19]. Indeed, although the mechanisms through which MHC influences odour and mate choice remain disputed [27], a recent meta-analysis, summarizing decades of research on vertebrate species, and in particular, in mammals, birds, fishes and reptiles, supports a female preference for MHC-diverse males and a preference for MHC dissimilarity when dissimilarity is characterized across multiple loci [28]. Preference for MHC-diverse males could provide direct benefits to females (healthier mates), as well as indirect genetic benefits to the offspring (rare beneficial alleles are more likely to be carried by MHC-diverse individuals and to be transmitted to the next generation). ...
... Because the dissimilarity among Dutch and more generally Northern European couples was MHC-specific and not found at the genome-wide level, it may result from MHC disassortative mating in these populations, possibly triggered by our olfactory capacity to discriminate MHC-mediated odours [18,22,27]. We explored the pattern of spouse dissimilarity throughout the MHC using a sliding-window approach and observed that the genetic dissimilarity among spouses was distributed all along the MHC, rather than localized to particular parts of the MHC, which suggests that such disassortative mating might be driven by a summation of effects over multiple genes (electronic supplementary material, figure S5). ...
Although pervasive in many animal species, the evidence for major histocompatibility complex (MHC) disassortative mating in humans remains inconsistent across studies. Here, to revisit this issue, we analyse dense genotype data for 883 European and Middle Eastern couples. To distinguish MHC-specific effects from socio-cultural confounders, the pattern of relatedness between spouses in the MHC region is compared to the rest of the genome. Couples from Israel exhibit no significant pattern of relatedness across the MHC region, whereas across the genome, they are more similar than random pairs of individuals, which may reflect social homogamy and/or cousin marriages. On the other hand, couples from The Netherlands and more generally from Northern Europe are significantly more MHC-dissimilar than random pairs of individuals, and this pattern of dissimilarity is extreme when compared with the rest of the genome. Our findings support the hypothesis that the MHC influences mate choice in humans in a context-dependent way: MHC-driven preferences may exist in all populations but, in some populations, social constraints over mate choice may reduce the ability of individuals to rely on such biological cues when choosing their mates.
... As every individual MHC allele recognizes only a subset of pathogens, MHC heterozygosity provides individuals the advantage of being resistant to a broader spectrum of diseases (Murphy, Janeway, Travers, Walport, & Ehrenstein, 2008). Therefore, based on the "heterozygote advantage" hypothesis, preferences for MHC-dissimilar partners maximize the likelihood of MHC-heterozygous progeny, which consequently results in fitness benefits (Penn & Potts, 1998a, 1998bPotts & Wakeland, 1990). Because the main function of the MHC proteins is the recognition of self and nonself (Janeway et al., 2004;Milinski, 2006), MHC-disassortative mating has been proposed as a mechanism to avoid inbreeding (Tregenza & Wedell, 2000). ...
... In many species, olfactory signals are used to assess MHC genotypes of conspecifics (Brown & Eklund, 1994;Olsson et al., 2003;Ruff et al., 2012;Wedekind et al., 1995;Yamazaki et al., 1979). Most of our knowledge about olfactory kin and mate recognition in vertebrates stems from research on humans and other mammalians (Brown, Roser, & Singh, 1989;Penn & Potts, 1998b, 1998cWedekind et al., 1995;Yamazaki et al., 1983Yamazaki et al., , 1976. As early as 1976, Yamazaki et al. (1976) presented convincing evidence that the MHC, which is an essential part of the immune system and their peptide ligands, are present in the odor profile of an individual (Boehm & Zufall, 2006;Leinders-Zufall et al., 2004;Singh, Brown, & Roser, 1987) and these cues are part of the individual's olfactory identity. ...
We here review the role of olfaction in the Zebra Finch, a key avian model species. We summarize the use of olfaction in social communication and in nonsocial contexts; its impact in addition to other senses throughout life; and how olfaction is involved in kin recognition, mate choice, and inbreeding avoidance. Afterward we explore the mechanisms of the olfactory signal and potential ways of signal production. We review olfactory signal production in avian species, the influences from the genome, and potential impact of skin microbes on scent production. This is followed by a paragraph on the perception and processing of the olfactory signal, from olfactory receptor genes, the olfactory bulb to the neural pathways in the songbird brain. Finally, we summarize several methods to examine olfaction in Zebra Finches on both, the behavioral level as well as on the chemical structural level. Based on the reviewed contents, we provide an outlook to future directions of each of the research fields to gather a further understanding of the use and the function as well as of the underlying mechanisms of olfaction in the Zebra Finch.
... In mammals, fish and seabirds, groups with well-developed chemical communication, receivers identify specific (e.g. locally rare) MHC alleles through olfactory cues from sweat, urine or preen oil [8][9][10]. Conversely, because individual diversity at MHC affects disease resistance, condition-dependent ornaments may signal MHC diversity [11,12]. ...
... MHC-related mating preferences have been observed in all vertebrate classes [3], raising the question of how animals assess MHC profiles. Cues of compatibility and diversity are generally studied in the contexts of chemosignalling [8][9][10] and visual ornaments [6,11,12], respectively. We investigated birdsong, an acoustic ornament, as a signal of MHC class IIb dissimilarity to other individuals in the population (a proxy for locally rare genotypes), and individual genetic diversity. ...
The major histocompatibility complex (MHC) plays a key role in vertebrate immunity, and pathogen-mediated selection often favours certain allelic combinations. Assessing potential mates' MHC profiles may provide receivers with genetic benefits (identifying MHC-compatible mates and producing optimally diverse offspring) and/or material benefits (identifying optimally diverse mates capable of high parental investment). Oscine songbirds learn songs during early life, such that song repertoire content can reflect population of origin while song complexity can reflect early life condition. Thus birdsong may advertise the singer's genetic dissimilarity to others in the population (and, presumably, compatibility with potential mates), or individual genetic diversity (and thus condition-dependent material benefits). We tested whether song repertoire content and/or complexity signal MHC class IIβ dissimilarity and/or diversity in male song sparrows (Melospiza melodia). Pairwise dissimilarity in repertoire content did not predict MHC dissimilarity between males, suggesting that locally rare songs do not signal rare MHC profiles. Thus, geographical variation in song may not facilitate MHC-mediated inbreeding or outbreeding. Larger repertoires were associated with intermediate MHC diversity, suggesting intermediate rather than maximal MHC diversity is optimal. This could reflect trade-offs between resisting infection and autoimmune disorders. Song complexity may advertise optimal MHC diversity, a trait affecting disease resistance and capacity for parental care.
... The role of compounds produced by the major histocompatibility complex (MHC) as pheromone carriers and stabilisers that extend the life of scent marks has been reviewed by Hurst et al. 1998), as has their influence on mating preferences (Penn & Potts 1998b). One of the main areas of recent research has focused on how the MHC genes control odour expression, as reviewed by Boyse et al. (1987), Penn (2002), Beauchamp & Yamazaki (2003), Dulac & Torello (2003) Studies on both trained and untrained mice show that mice prefer to mate with individuals with different MHC alleles, and that this is mediated by odour ( Carroll et al. 2002;Spehr et al. 2006), providing a mechanism by which inbreeding can be avoided (Penn 2002). ...
... The interplay between the use of odours for social recognition and the disease status of individuals could be explored from the perspective of pest control. Mice not only detect conspecifics suffering from infectious diseases based on their social odours, but also use this information in mate choice (Penn & Potts 1998b;Penn et al. 1998;Beauchamp & Yamazaki 2003;Lopes & K?nig 2016). Similarly, rodents select mates that are not infected by parasites ( Kavaliers et al. 2003aKavaliers et al. ,b, 2005Zala et al. 2004;Gerlinskaya et al. 2012). ...
To improve conservation outcomes and move towards a ‘predator-free New Zealand’, we need new pest control technologies. Our growing knowledge of the chemistry, behaviour and neuroendocrinology of mammalian scents that affect other individuals (semiochemicals) provides an opportunity for these to be used in various ways to help to control pest species. In this report, we summarise current knowledge of attractant semiochemicals (pheromones) of rodents, mustelids, cats and possums in New Zealand, to find potential avenues for the development of lures and other control strategies. Putative pheromones have been identified in all these species, and the major urinary proteins (MUPs) and peptides derived from the major histocompatibility complex (MHC) have been shown to play a role as pheromone carriers in the house mouse (Mus musculus), Norway rat (Rattus norvegicus) and ship rat (R. rattus). In addition, attractant compounds have been identified in the urine and glands of cats (Felis catus), mustelids (stoats – Mustela erminea, weasels – M. nivalis and ferrets – M. furo) and brushtail possums (Trichosurus vulpecula), and the calming effect of the feline facial pheromone has been explored. There are several potential applications for pheromones in mammalian pest management, including in trap and lure-and-kill systems; toxic baits; immunocontraception or chemosterilisation delivery systems; monitoring for incursions; interruption of breeding behaviour; and enhancement of biological control. The learned component of responses to pheromones and the role of MUPs in that learning suggest a complex system and it is unlikely that there will be a single ‘magic bullet’ solution for all pest species, but some potential for inter-species attractants. The use of novel control strategies based on a sound understanding of animal behaviour and neurophysiology could see pheromones and MUPs being combined to help improve predator control in New Zealand.
... Identical twins living in different environments may share the same primary odor but not necessarily the same secondary odor. The MHC influence can be described by three different hypotheses (48). First, MHC molecules may directly be found in human sweat and therefore may be part of human odor. ...
... There are up to 500 different species on a living person and c. 10 species representing 50% of the skin microflora. According to the authors (46,(48)(49)(50), it is more likely that a combination of these hypotheses may provide a plausible explanation. The MHC would bind to specific subsets of peptides that may be conveyed to glands where bacterial actions produce volatile and odoriferous metabolites. ...
The use of comprehensive two-dimensional gas chromatography coupled with mass spectrometry would be a real asset for the forensic profiling of human hand odor. This paper focuses on the optimization of a comprehensive gas chromatography method using a synthetic mixture of 80 compounds representative of human hand odor composition. In order to rank the candidate column sets, instead of using a unique criterion, we used a chemometric tool called desirability which is based on Derringer functions and enables to consider several criteria simultaneously and hence to get the best compromise. Nine criteria including six orthogonality criteria were used to evaluate the quality and the efficiency of the separation. The desirability analysis lead to a straightforward ranking and an accurate overview of the results in two situations, with an objective of routine analysis and without. In both cases, the DB-1MS×DB-1701 set was found to be best suited for the separation of the considered mixture, however with different gradients.
... Due to a high diversity of MHC I encoding genes, the existence of two identical odourtypes is highly unlikely. The way of detecting MHC was conserved during the evolution and is present in all mammalian species[Boehm and Zufall 2006, Kwak et al. 2009, Penn and Potts 1997, Restrepo et al. 2006. The schematic method of MHC I peptide ligand detection is shown inFigure 1. ...
... The authors suggested that it provided evidence that bank voles use MHC-related cues to choose compatible mates. Generally the results of the research carried on rodents support the hypothesis that mate choice is MHC-depended, as well as the fact that in most cases it is the female that chooses a mate [Potts 1997, Penn andPotts 1999]. ...
Reproduction is one of the basic biological functions in animals and humans. Due to the high biological relevance of reproduction and energy investment in their rearing offspring need to be of the best genetic quality and tness to ensure preservation of the species. Both males and females employ mating strategies that would promote reproduction success and survival of their offspring. Choosing a high-quality mating partner is considered to be the main strategy in the reproduction process. One of the factors in uencing the partner’s attractiveness is Major Histocompatibility Complex class I (MHC I). The in uence of MHC I on mate choice is well established in animals, whereas it is still questioned in humans, where the social status of a partner may strongly in uence the mate choice. In this review the role of the MHC1 on mate choice in animals and humans is discussed. The studies published so far show that all investigated mammalian species can detect fractions of the MHC I molecules in urine and other body uids. The response to the signal carried by MHC I is context-dependent and varies not only between species, but also between genders and may be modulated by various socioecological factors in every phase of the reproduction process, until zygote formation. These results suggest that MHC plays an important role in the choice of a reproductive partner in all mammal species, including humans.
... Identical twins living in different environments may share the same primary odor but not necessarily the same secondary odor. The MHC influence can be described by three different hypotheses (48). First, MHC molecules may directly be found in human sweat and therefore may be part of human odor. ...
... There are up to 500 different species on a living person and c. 10 species representing 50% of the skin microflora. According to the authors (46,(48)(49)(50), it is more likely that a combination of these hypotheses may provide a plausible explanation. The MHC would bind to specific subsets of peptides that may be conveyed to glands where bacterial actions produce volatile and odoriferous metabolites. ...
Developing a strategy to characterize the odor prints of individuals should be relevant to support identification obtained using dogs in courts of justice. This article proposes an overview of the techniques used for the forensic profiling of human odor. After reviewing the origin of human odor-both genetic and physiological-the different analytical steps from sample collection to statistical data processing are presented. The first challenge is the collection of odor, whether by direct sampling with polymer patches, cotton gauze, etc., or indirect sampling with devices like Scent Transfer Unit. Then, analytical techniques are presented. Analyses are commonly performed with gas chromatography coupled with mass spectrometry. As they yield large amounts of data, advanced statistical tools are needed to provide efficient and reliable data processing, which is essential to give more probative value to information.
... Skin and feather bacteria are responsible for the transformation of sweat components to VOCs [174]. Because the presence of blood parasites may modify the odour of an individual by altering the profile of symbiotic microbial community [175], the infection with malaria parasites may result in increased attractiveness of hosts. In this sense, an increased attractiveness of malaria-infected hosts to mosquitoes has been shown in humans [170,174,176,177], rodents [178,179], and birds ( [52,54]; see review in [180]). ...
Vector-borne infectious diseases (e.g., malaria, dengue fever, and yellow fever) result from a parasite transmitted to humans and other animals by blood-feeding arthropods. They are major contributors to the global disease burden, as they account for nearly a fifth of all infectious diseases worldwide. The interaction between vectors and their hosts plays a key role driving vector-borne disease transmission. Therefore, identifying factors governing host selection by blood-feeding insects is essential to understand the transmission dynamics of vector-borne diseases. Here, we review published information on the physical and chemical stimuli (acoustic, visual, olfactory, moisture and thermal cues) used by mosquitoes and other haemosporidian vectors to detect their vertebrate hosts. We mainly focus on studies on avian malaria and related haemosporidian parasites since this animal model has historically provided important advances in our understanding on ecological and evolutionary process ruling vector-borne disease dynamics and transmission. We also present relevant studies analysing the capacity of feather and skin symbiotic bacteria in the production of volatile compounds with vector attractant properties. Furthermore, we review the role of uropygial secretions and symbiotic bacteria in bird–insect vector interactions. In addition, we present investigations examining the alterations induced by haemosporidian parasites on their arthropod vector and vertebrate host to enhance parasite transmission. Finally, we propose future lines of research for designing successful vector control strategies and for infectious disease management.
... Learning in the context of reproductive behaviours, that is, a change in the future sexual behaviour of an individual as a result of previous social experience ( Thorpe et al., 1963;Gailey et al., 1982;Dukas, 2005b;Barron et al., 2015), has been seen in both vertebrates and invertebrates (reviewed in Dion et al., 2019). In vertebrates, examples of these learned sexual behaviours include 'sexual imprinting' which has been reported in various species of birds (Ten Cate & Vos, 1999;Slagsvold et al., 2002;Witte & Sawka, 2003;Cate et al., 2006), fishes (Verzijden et al., 2008) and mammals (Kendrick et al., 1998;Penn & Potts, 1998;Marcinkowska & Rantala, 2012;Griffee et al., 2017). Learning mate preferences from prior social experiences has also been demonstrated in a wide range of insect species. ...
Courtship is an important component of male reproductive behaviour that enables males to learn about the suitability of their mating partners. Experimental evidence suggests that Drosophila melanogaster males can learn to modify their courtship behaviour based on their prior experience with unreceptive females. This courtship learning is expected to provide a fitness advantage to males and could therefore evolve given suitable heritable variation. We investigated the role of sexual selection in the evolution of courtship learning ability of males, using populations of D. melanogaster evolving under high and low levels of sexual selection for over 170 generations. We exposed males from both types of population to unreceptive females and then tested their ability to discriminate between receptive and unreceptive females in a complex mating environment. After being exposed to unreceptive females, males from both types of population (1) courted females less (both receptive and unreceptive), (2) took longer to initiate courtship, but took less time to start mating after initiating courtship and (3) increased the proportion of courtship directed towards receptive females, indicating the ability of both types of males to learn from previous experience. We did not find any difference in the courtship learning ability of males from the two types of populations. However, males from populations with higher levels of sexual selection were better at recognizing and courting receptive females, even when they were not previously exposed to unreceptive females. Taken together, these results show that sexual selection may not result in improved learning abilities but can lead to the evolution of an improved innate ability of males to assess the receptivity of females.
... Notably, one of the fundamental tenets of adaptive immune systems is self-tolerance: somatically recombined receptors that bind host proteins are deleted during lymphocyte development. This process is mediated by proteins within the MHC and has been proposed to have been co-opted from an ancient olfactory system still used in mate choice based on peptide carrier protein phenotype (Andreou et al., 2017;Boehm, 2006;Penn and Potts, 1998). Even after negative selection to eliminate receptors that bind self-antigens, the adaptive immune system is a powerful, lethal tool in vertebrates that requires tight regulation. ...
Detecting danger is key to the survival and success of all species. Animal nervous and immune systems cooperate to optimize danger detection. Preceding studies have highlighted the benefits of bringing neurons into the defense game, including regulation of immune responses, wound healing, pathogen control, and survival. Here, we summarize the body of knowledge in neuroimmune communication and assert that neuronal participation in the immune response is deeply beneficial in each step of combating infection, from inception to resolution. Despite the documented tight association between the immune and nervous systems in mammals or invertebrate model organisms, interdependence of these two systems is largely unexplored across metazoans. This review brings a phylogenetic perspective of the nervous and immune systems in the context of danger detection and advocates for the use of non-model organisms to diversify the field of neuroimmunology. We identify key taxa that are ripe for investigation due to the emergence of key evolutionary innovations in their immune and nervous systems. This novel perspective will help define the primordial principles that govern neuroimmune communication across taxa.
... The major histocompatibility complex, or MHC, is a family of highly polymorphic immune genes found in all vertebrates (Iwasaki and Medzhitov 2010). It is thought to be the primary genetic determinant of personal odor (Penn and Potts 1998;Yamazaki et al. 1976) and it has been implicated in facilitating individual discrimination in all classes of vertebrates (Fish: Milinski 2006;Reusch et al. 2001;Reptiles: Olsson et al. 2003;Birds: Grieves et al. 2019b;Leclaire et al. 2017b;Mammals: Potts et al. 1991;Wedekind and Penn 2000;Yamazaki et al. 1976). Furthermore, since MHC reflects the quality of the immune system, it is also expected to play a key role in mate choice (Boehm and Zufall 2006;Penn 2002;Penn and Potts 1999). ...
Avian chemical communication, once largely overlooked, is a growing field that has revealed the important role that olfaction plays in the social lives of some birds. Leach’s storm-petrels (Oceanodroma leucorhoa) have a remarkable sense of smell and a strong, musky scent. This long-lived, monogamous seabird relies on olfaction for nest relocation and foraging, but whether they use scent for communication is less well studied. They are nocturnally active at the breeding colony and yet successfully reunite with their mate despite poor night-vision, indicating an important role for non-visual communication. We investigated the chemical profiles of Leach’s storm-petrels to determine whether there is socially relevant information encoded in their plumage odor. To capture the compounds comprising their strong scent, we developed a method to study the compounds present in the air surrounding their feathers using headspace stir bar sorptive extraction coupled with gas chromatography-mass spectrometry. We collected feathers from Leach’s storm-petrels breeding on Bon Portage Island in Nova Scotia, Canada in both 2015 and 2016. Our method detected 142 commonly occurring compounds. We found interannual differences in chemical profiles between the two sampling years. Males and females had similar chemical profiles, while individuals had distinct chemical signatures across the two years. These findings suggest that the scent of the Leach’s storm-petrel provides sociochemical information that could facilitate olfactory recognition of individuals and may inform mate choice decisions.
... Heterozygosity also appears to have implications for mate choice, such that individuals may prefer MHCdissimilar mates in order to increase offspring heterozygosity. Dissimilarity preferences have been found across a range of non-human animals [32][33][34][35][36] , and some work suggests MHC-dissimilarity is associated with higher fecundity (e.g., 1,2 ). In humans, some studies suggest that members of MHC-similar romantic couples are less sexually responsive to their partners and report higher levels of extra-pair attraction 37,38 . ...
Although allelic diversity at the major histocompatibility complex (MHC) has implications for adaptive immunity, mate choice, and social signalling, how diversity at the MHC influences the calibration of life history strategies remains largely uninvestigated. The current study investigated whether greater MHC heterozygosity was associated with markers of slower life history strategies in a sample of 789 North American undergraduates. Contrary to preregistered predictions and to previously published findings, MHC heterozygosity was not related to any of the psychological life history-relevant variables measured (including short- vs. long-term sexual strategy, temporal discounting, the Arizona life history battery, past and current health, disgust sensitivity, and Big Five personality traits). Further, no meaningful effects emerged when analysing women and men separately. Possible reasons for why the current results are inconsistent with previous work are discussed.
... The specialized secretions in (e) contribute additional organic compounds to those present in bladder urine [32] and in ( f ), shown as crystallized exudate, activate a venom when mixed with saliva, producing a poisonous bite [33,34]. and determining histocompatibility [63] and has a wellknown influence over an individual's odour [64]. Otherwise, the fermentation hypothesis posits that symbiotic bacteria play a crucial role in producing volatile organic compounds (VOCs) used in chemical communication [65]. ...
The study of human chemical communication benefits from comparative perspectives that relate humans, conceptually and empirically, to other primates. All major primate groups rely on intraspecific chemosignals, but strepsirrhines present the greatest diversity and specialization, providing a rich framework for examining design, delivery and perception. Strepsirrhines actively scent mark, possess a functional vomeronasal organ, investigate scents via olfactory and gustatory means, and are exquisitely sensitive to chemically encoded messages. Variation in delivery, scent mixing and multimodality alters signal detection, longevity and intended audience. Based on an integrative, 19-species review, the main scent source used (excretory versus glandular) differentiates nocturnal from diurnal or cathemeral species, reflecting differing socioecological demands and evolutionary trajectories. Condition-dependent signals reflect immutable (species, sex, identity, genetic diversity, immunity and kinship) and transient (health, social status, reproductive state and breeding history) traits, consistent with socio-reproductive functions. Sex reversals in glandular elaboration, marking rates or chemical richness in female-dominant species implicate sexual selection of olfactory ornaments in both sexes. Whereas some compounds may be endogenously produced and modified (e.g. via hormones), microbial analyses of different odorants support the fermentation hypothesis of bacterial contribution. The intimate contexts of information transfer and varied functions provide important parallels applicable to olfactory communication in humans.
This article is part of the Theo Murphy meeting issue ‘Olfactory communication in humans’.
... For mating and social behavior to be influenced by the MHC, however, individuals must both indicate their respective MHC genotype and be able to evaluate the MHC information in the signals of conspecifics [8,47]. Previously, researchers have shown that condition-dependent signals of quality can be used by both sexes to assess potential partners [18,54,89,90]. Although evidence of correlation with MHC genotype has derived primarily from visual signals, such as antler size [25] or bright coloration [107], chemical signals could prove more reliable for advertising MHC genotype [7,74,88,126]: Notably, because degraded MHC molecules are shed from the cell surface and found in body fluids (e.g. ...
Background
Diversity at the Major Histocompatibility Complex (MHC) is critical to health and fitness, such that MHC genotype may predict an individual’s quality or compatibility as a competitor, ally, or mate. Moreover, because MHC products can influence the components of bodily secretions, an individual’s body odors may signal its MHC composition and influence partner identification or mate choice. Here, we investigated MHC-based signaling and recipient sensitivity by testing for odor-gene covariance and behavioral discrimination of MHC diversity and pairwise dissimilarity in a strepsirrhine primate, the ring-tailed lemur (Lemur catta).
Methods
First, we coupled genotyping of the MHC class II gene, DRB, with gas chromatography-mass spectrometry of genital gland secretions to investigate if functional genetic diversity is signaled by the chemical diversity of lemur scent secretions. We also assessed if the chemical similarity between individuals correlated with their MHC-DRB similarity. Next, we assessed if lemurs discriminated this chemically encoded, genetic information in opposite-sex conspecifics.
Results
We found that both sexes signaled overall MHC-DRB diversity and pairwise MHC-DRB similarity via genital secretions, but in a sex- and season-dependent manner. Additionally, the sexes discriminated absolute and relative MHC-DRB diversity in the genital odors of opposite-sex conspecifics, suggesting that lemur genital odors function to advertise genetic quality.
Conclusions
In summary, genital odors of ring-tailed lemurs provide honest information about an individual’s absolute and relative MHC quality. Complementing evidence in humans and Old World monkeys, we suggest that reliance on scent signals to communicate MHC quality may be important across the primate lineage.
... Alleles of the major histocompatibility complex (Mhc) can have both direct and indirect effects on the odour of animals (Penn and Potts, 1998), and mating preferences for individuals with odour cues associated with complementary Mhc genotypes, which confer maximum Mhc heterozygosity, and hence protection against a range of infections, on resulting offspring (Penn et al., 2002), are used as mate choice criteria in mice (Potts et al., 1991) and humans (Wedekind et al., 1995). Recent studies on three-spined sticklebacks have also demonstrated Mhc-based odour cues to play an important role in mate choice in fish, with preferences apparently arising because resultant Mhc genotypes confer anti-parasite benefits on offspring. ...
Parasites1 are ubiquitous components of natural and managed ecosystems. Water provides a particularly suitable medium for the support and movement of directly transmitted ectoparasites, and the central role played by fish in aquatic food webs make them ideal intermediate hosts for indirectly transmitted infections. Consequently, parasites use fish as hosts. By definition, parasite infections negatively impact host fish, though very often these detrimental effects are unquantified. However, parasites rely on their hosts for nutrition; so they impose at least energetic demands, and very often they have other physiological impacts. Parasites can be classified as environmental stressors of fish, not only because of the direct impacts they impose after infection, but also because their presence in aquatic environments can reduce the efficiency with which fishes function. The latter effects may arise because of constraints imposed on, for example, the habitat selection or food selection choices that are available to fish attempting to avoid contact with infectious agents.
... Considering the composition and structure of the microbial communities are influenced by hosttraits such as phylogeny, social interactions, diet and health status, microbes may broadcast information about the host individuals and therefore be used in social communication [8]. This relationship is quite obvious and well documented for certain infections, which come along with specific odours in humans and other mammals [120,121]. This information about the current health status is very important and can alter mate choice decisions in mice [122]. ...
Animal bodies harbour a complex and diverse community of microorganisms and accumulating evidence has revealed that microbes can influence the hosts’ behaviour, for example by altering body odours. Microbial communities produce odorant molecules as metabolic by-products and thereby modulate the biochemical signalling profiles of their animal hosts. As the diversity and the relative abundance of microbial species are influenced by several factors including host-specific factors, environmental factors and social interactions, there are substantial individual variations in the composition of microbial communities. In turn, the variations in microbial communities would consequently affect social and communicative behaviour by influencing recognition cues of the hosts. Therefore, microbiota studies have a great potential to expand our understanding of recognition of conspecifics, group members and kin. In this review, we aim to summarize existing knowledge of the factors influencing the microbial communities and the effect of microbiota on olfactory cue production and social and communicative behaviour. We concentrate on avian taxa, yet we also include recent research performed on non-avian species when necessary.
... They showed that the volatiles from individuals in an identical twin pair showed a significantly higher correlation in attractiveness to mosquitoes than the , nonidentical twin pairs (Fernández-Grandon et al., 2015). Although it is not known which genes are responsible for this correlation, the human leukocyte antigen genes may be good candidates as they have shown to influence mice and human body odor (Penn and Potts, 1998;Wedekind and Furi, 1997), and a tentative link was found in another study (Verhulst et al., 2013a). ...
Despite acting as a highly efficient barrier against surface pathogenic microbes, the skin is still the major portal of entry for most arthropod-borne pathogens. Proper understanding of the mechanisms by which these microbial agents circumvent the skin defenses is a critical step in the development of new strategies to fight these major threats to human health. In this chapter, a comprehensive overview of the human skin immune system organization is depicted, providing up-to-date knowledge on the main cellular actors of both the innate and adaptive immunity populating this large organ. The rather scarce data about the skin inflammatory response to vector-competent arthropod bite are also presented.Finally, because accumulating evidence demonstrates an essential role of the human skin microbiome in homeostasis and in defense against pathogens, an overview of its diversity and functions is provided, giving interesting perspectives on its possible implications in arthropod-borne pathogens transmission.
... are responsible for this correlation, the human leukocyte antigen genes may be good candidates as they have shown to influence mice and human body odor (Penn and Potts, 1998;Wedekind and Furi, 1997), and a tentative link was found in another study (Verhulst et al., 2013a). ...
Many hematophagous arthropods are vectors of diseases. They find their host using a range of cues, of which carbon dioxide is often crucial. Especially for arthropods that have a specific host preference, skin volatiles play an important role when they search for their host. By volatile collection followed by gas chromatography, hundreds of skin volatiles can be identified of which a large subset is produced by skin bacteria. The olfactory response of the arthropod to these compounds can be evaluated with electroantennograms, in olfactometers and (semi-)field settings. The identification and evaluation of these compounds has led to the development of novel attractants or repellents and can be used in vector monitoring and intervention programs. More recently, the skin microbiome has been shown to play a role in the attractiveness of a host to arthropods by the metabolome released by resident skin bacteria. The microbiota might also be important on the direct transmission of pathogens by arthropods at the skin interface. This second aspect is largely unexplored.
... Across animal species, olfaction is known to play a key role in social communication and mating behavior (Wyatt, 2003). While human capacity for olfactory communication has been considered weak in relation to most mammals, it is well known that in many animal species (e.g.,mice), social communication and mate choice are influenced by cues encoded by the Major Histocompatibility Complex (MHC, called Human Leucocyte Antigen, or HLA in humans), a gene cluster that constitutes the main factor in determining immunological individuality (e.g., Penn & Potts, 1998). Similarly to other species, humans are thought to partially base their choice of a partner on their genetic potential, exhibiting preferences for the odor of individuals who are dissimilar from themselves at genes coded in the HLA, thus striving for genetic variability and a more resistant immunity system Jacob, McClintock, Zelano, & Ober, 2002 , 2016;Wedekind & Füri, 1997;Wedekind, Seebeck, Bettens, & Paepke, 1995). ...
Olfaction is often linked to mating behavior in nonhumans. Additionally, studies in mating behavior have shown that women seem to be more affected by odor cues than men. However, the relationship between odor cues and sexual response - specifically, sexual arousal - has not been studied yet. The aim of this study was to evaluate the impact of the exposure to human body odors (from individuals of the opposite gender) on perceived genital arousal, while these were presented concomitantly to sexually explicit video clips. Eighty university students (40 women) rated their perceived genital arousal (perceived degree of erection/genital lubrication) in response to an audiovisual sexual stimulus, while simultaneously exposed to a body odor from an opposite gender donor or no odor. Participants also rated each odor sample's (body odor and no odor) perceived pleasantness, intensity, and familiarity. Findings indicated that odor condition had an effect on women's (but not men's) perceived genital arousal, with women showing higher levels of perceived genital arousal in the no odor condition. Also, results showed that women rated body odors as less pleasant than no odor. Notwithstanding, the odor ratings do not seem to explain the association between body odor and perceived genital arousal. The current results support the hypothesis that women, rather than men, are sensitive to odors in the context of sexual response. The findings of this study have relevance for the understanding of human sexuality with respect to
chemosensory communication.
... Bacterial Hypothesis: Do Skin Microbiota Mediate Plasmodium-Induced Changes in Odour Profile? Penn and Potts [79] suggested that infection with parasites can change the odour of an individual by changing the profile of commensal microbes. During infection, the activities of either the immunological and/or endocrine systems may be induced by parasite infection. ...
Evidence is accumulating that Plasmodium-infected vertebrates are more attractive to mosquitoes than noninfected hosts, particularly when high levels of gametocytes are present. Changes in host odour have been suggested as a likely target for parasite manipulation because olfactory cues are crucial to mosquitoes in search of a bloodmeal host. This review discusses two routes that may lead to such changes: (i) direct emission of volatile products from malaria parasites, and (ii) changes in skin microbial composition that could lead to changes in the vertebrate odour profile. Here we synthesize what is known and suggest how further research can increase our understanding of the mechanisms of parasite manipulation of host attractiveness.
... The major histocompatibility complex (MHC) molecules can bind peptide fragments derived from pathogens and present them on the cell surface for recognition by the appropriate T cells. MHC genes are linked to reproductive and social behaviours such as mate choice and kin selection (Penn and Potts, 1998;Janssen and Zavazava, 1999;Jacob et al., 2002). According to a Setchell et al. (2011) study on the Old World monkey, odour provides a cue of individual genetic quality as well as information against which the receiver can compare its own genotype to assess genetic similarity. ...
In the 20th century, mother-infant separation shortly after birth in hospitals became routine and unique to humans. However, this hospital birth practice is different from the practice in our evolutionary history, where newborn survival depended on close and essentially continuous maternal contact. This time shortly after birth represents a psychophysiologically sensitive or critical period for programming future physiology and behaviour. We hypothesize that early maternal separation as conducted in conventional hospital practice may induce similar epigenetic changes similar to those found in various mental diseases that may also be implicated in neurodevelopmental disorders.
... The control of mammalian body odour production, which may mediate attractiveness to mosquitoes, has been linked to MHC genes (41), which encode cell-surface glycoproteins that present peptides to antigen receptors of T cells, an interaction pivotal for the maintenance of self-tolerance, and protection against pathogens and tumours (42). It is these MHC-derived peptides that undergo metabolism by skin microflora to produce a particular composition of odour (43,44). ...
Understanding the interaction between humans and mosquitoes is a critical area of study due to the phenomenal burdens on public health from mosquito-transmitted diseases.
In this study we conducted the first genome-wide association studies (GWAS) of self-reported mosquito bite reaction size (n = 84,724), itchiness caused by bites (n = 69,057), and perceived attractiveness to mosquitoes (n = 16,576). In total, 15 independent significant (P<5x10⁻⁸) associations were identified. These loci were enriched for immunity-related genes that are involved in multiple cytokine signalling pathways. We also detected suggestive enrichment of these loci in enhancer regions that are active in stimulated T-cells, as well as within loci previously identified as controlling central memory T-cell levels. Egger regression analysis between the traits suggests that perception of itchiness and attractiveness to mosquitoes is driven, at least in part, by the genetic determinants of bite reaction size.
Our findings illustrate the complex genetic and immunological landscapes underpinning human interactions with mosquitoes.
... Nevertheless, mate choice based directly upon infection status does still occur. Laboratory and captive rodents are consistently observed to avoid mating with individuals infected with parasitic nematodes, viruses, and other microorganisms (Penn and Potts 1998b;Zala et al. 2004;Kavaliers et al. 2005a). In rodents, olfactory signals appear to allow mate discrimination on the basis of infection Potts 1998 a, 1998b;Gosling and Roberts 2001;Arakawa et al. 2011). ...
Preference for uninfected mates is presumed beneficial as it minimizes one’s risk of contracting an infection and infecting one’s offspring. In avian systems, visual ornaments are often used to indicate parasite burdens and facilitate mate-choice. However, in mammals, olfactory cues have been proposed to act as a mechanism allowing potential mates to be discriminated by infection status. The effect of infection upon mammalian mate-choice is mainly studied in captive rodents where experimental trials support preference for the odors of uninfected mates and some data suggest scent marking is reduced in individuals with high infection burdens. Nevertheless, whether such effects occur in non-model and wild systems remains poorly understood. Here we investigate the interplay between parasite load (estimated using fecal egg counts) and scent marking behavior in a wild population of banded mongooses, Mungus mungo. Focusing on a costly protozoan parasite of the genus Isospora and the nematode worm Toxocara, we first show that banded mongooses that engage in frequent, intensive scent-marking have lower Isospora loads, suggesting marking behavior may be an indicator trait regarding infection status. We then use odor presentations to demonstrate that banded mongooses mark less in response to odors of opposite-sexed individuals with high Isospora and Toxocara loads. As both of these parasites are known to have detrimental effects upon the health of pre-weaned young in other species, they would appear key targets to avoid during mate-choice. Results provide support for scent as an important ornament and mechanism for advertising parasitic infection within wild mammals.
... In addition, it has been suggested that MHC molecules influence microorganisms of the skin which are involved in the formation of body odours 7 . The precise mechanisms by which those MHC molecules shape the body odor are still under discussion 8 . However, MHC determined odors activate vomeronasal and olfactory neurons 4 . ...
The major histocompatibility complex (MHC, called HLA in humans) is an important genetic component of the immune system. Fish, birds and mammals prefer mates with different genetic MHC code compared to their own, which they determine using olfactory cues. This preference increases the chances of high MHC variety in the offspring, leading to enhanced resilience against a variety of pathogens. Humans are also able to discriminate HLA related olfactory stimuli, however, it is debated whether this mechanism is of behavioural relevance. We show on a large sample (N = 508), with high-resolution typing of HLA class I/II, that HLA dissimilarity correlates with partnership, sexuality and enhances the desire to procreate. We conclude that HLA mediates mate behaviour in humans.
The Cambridge Handbook of Political Psychology provides a comprehensive review of the psychology of political behaviour from an international perspective. Its coverage spans from foundational approaches to political psychology, including the evolutionary, personality and developmental roots of political attitudes, to contemporary challenges to governance, including populism, hate speech, conspiracy beliefs, inequality, climate change and cyberterrorism. Each chapter features cutting-edge research from internationally renowned scholars who offer their unique insights into how people think, feel and act in different political contexts. By taking a distinctively international approach, this handbook highlights the nuances of political behaviour across cultures and geographical regions, as well as the truisms of political psychology that transcend context. Academics, graduate students and practitioners alike, as well as those generally interested in politics and human behaviour, will benefit from this definitive overview of how people shape – and are shaped by – their political environment in a rapidly changing twenty-first century.
This chapter discusses some of the relevant findings in the study of genetics and politics, with an examination of how these forces interact and intersect. Particular attention is given to the importance of assortative mating in determining political ideology, a topic that has been typically neglected by political science. Full incorporation of evolutionary, biological, and genetic contributions to political attitudes, preferences, and behaviour should start to change the way we think about both politics and science. Environments are not infinitely malleable and susceptible to easy intervention, any more than biology or genetics are immutable, fixed, or unchanging. Our genes operate in a social context and constantly interact with that environment in a recursive and iterative manner. These mechanisms also influence how we get our genes through processes like mate selection, and affect how those genes operate in a complex social and political world. This interaction has real-world political and social consequences, producing significant outcomes, including in-group protection, out-group discrimination, allocation of resources, and the regulation of human sexuality in all forms.
The house mouse is the source of almost all genetic variation in laboratory mice; its genome was sequenced alongside that of humans, and it has become the model for mammalian speciation. Featuring contributions from leaders in the field, this volume provides the evolutionary context necessary to interpret these patterns and processes in the age of genomics. The topics reviewed include mouse phylogeny, phylogeography, origins of commensalism, adaptation, and dynamics of secondary contacts between subspecies. Explorations of mouse behaviour cover the nature of chemical and ultrasonic signalling, recognition, and social environment. The importance of the mouse as an evolutionary model is highlighted in reviews of the first described example of meiotic drive (t-haplotype) and the first identified mammalian speciation gene (Prdm9). This detailed overview of house mouse evolution is a valuable resource for researchers of mouse biology as well as those interested in mouse genetics, evolutionary biology, behaviour, parasitology, and archaeozoology.
The house mouse is the source of almost all genetic variation in laboratory mice; its genome was sequenced alongside that of humans, and it has become the model for mammalian speciation. Featuring contributions from leaders in the field, this volume provides the evolutionary context necessary to interpret these patterns and processes in the age of genomics. The topics reviewed include mouse phylogeny, phylogeography, origins of commensalism, adaptation, and dynamics of secondary contacts between subspecies. Explorations of mouse behaviour cover the nature of chemical and ultrasonic signalling, recognition, and social environment. The importance of the mouse as an evolutionary model is highlighted in reviews of the first described example of meiotic drive (t-haplotype) and the first identified mammalian speciation gene (Prdm9). This detailed overview of house mouse evolution is a valuable resource for researchers of mouse biology as well as those interested in mouse genetics, evolutionary biology, behaviour, parasitology, and archaeozoology.
Social signals can serve as potent emotional triggers with powerful impacts on processes from cognition to valence processing. How are social signals dynamically and flexibly associated with positive or negative valence? How do our past social experiences and present social standing shape our motivation to seek or avoid social contact? We discuss a model in which social attributes, social history, social memory, social rank and social isolation can flexibly influence valence assignment to social stimuli, termed here as ‘social valence’. We emphasize how the brain encodes each of these four factors and highlight the neural circuits and mechanisms that play a part in the perception of social attributes, social memory and social rank, as well as how these factors affect valence systems associated with social stimuli. We highlight the impact of social isolation, dissecting the neural and behavioural mechanisms that mediate the effects of acute versus prolonged periods of social isolation. Importantly, we discuss conceptual models that may account for the potential shift in valence of social stimuli from positive to negative as the period of isolation extends in time. Collectively, this Review identifies factors that control the formation and attribution of social valence — integrating diverse areas of research and emphasizing their unique contributions to the categorization of social stimuli as positive or negative. Social valence — the valence assigned to a social agent or social stimulus — is complex to compute. In this Review, Padilla-Coreano et al. explain how social attributes, social history, social memory, social rank and social isolation states are integrated to modulate social valence assignment.
Inbreeding and low diversity in MHC genes are considered to have a negative effect on reproductive success in animals. This study presents an analysis of the number and body mass of offspring in domestic cat, depending on the inbreeding coefficient and the degree of similarity in MHC genes of class I and II in parents. Inbred partners had a lower number of live kittens at birth than outbred ones. At the same time, the inbreeding coefficient did not affect the litter size and the number of offspring who survived until the period of transition to solid food. The most significant predictor for the number of surviving offspring was the degree of parental similarity in MHC genes: the parents with the maximum distance in MHC genes had more survived kittens. Moreover, this effect was most pronounced immediately after birth. A significant percentage of kittens from parents with a minimum distance in MHC genes were either stillborn or died on the first day after birth. By the age of transition to solid food, this effect is no longer so pronounced. Furthermore, neither the inbreeding coefficient nor the distance in MHC genes of parents had any effect on the body mass of kittens.
Skin is the largest mammalian organ and the first defensive barrier against the external environment. The skin and fur of mammals can host a wide variety of ectoparasites, many of which are phylogenetically diverse, specialized, and specifically adapted to their hosts. Among hematophagous dipteran parasites, volatile organic compounds (VOCs) are known to serve as important attractants, leading parasites to compatible sources of blood meals. VOCs have been hypothesized to be mediated by host‐associated bacteria, which may thereby indirectly influence parasitism. Host‐associated bacteria may also influence parasitism directly, as has been observed in interactions between animal gut microbiota and malarial parasites. Hypotheses relating bacterial symbionts and eukaryotic parasitism have rarely been tested among humans and domestic animals, and have to our knowledge never been tested in wild vertebrates. In this study, we use Afrotropical bats, hematophagous ectoparasitic bat flies, and haemosporidian (malarial) parasites vectored by bat flies as a model to test the hypothesis that the vertebrate host microbiome is linked to parasitism in a wild system. We identify significant correlations between bacterial community composition of the skin and dipteran ectoparasite prevalence across four major bat lineages, as well as striking differences in skin microbial network characteristics between ectoparasitized and non‐ectoparasitized bats. We also identify links between the oral microbiome and presence of malarial parasites among miniopterid bats. Our results support the hypothesis that microbial symbionts may serve as indirect mediators of parasitism among eukaryotic hosts and parasites.
This chapter provides an examination of the parasite taxa that regularly infect threespined sticklebacks in natural environments and their impacts on host biology, with the aim of developing an understanding of their role as agents of natural and sexual selection in host populations. The taxonomic and life cycle diversity of stickleback parasites is introduced, and patterns of infection in stickleback populations are examined. The various behavioural mechanisms that sticklebacks can use to avoid parasites or otherwise reduce their own risk of infection or that of their offspring are reviewed. The biology of infected fish is discussed, and sections are included that address the impact of infection on host morphology, physiology, growth, and sexual development. Many stickleback parasites also affect the behaviour of their hosts, and behavioural changes resulting from parasite infections can have potentially significant consequences for the ecology of host individuals and the evolution of populations. In some cases, parasites may actually benefit from the changes in behaviour they induce in their hosts. The impact of parasites on the behaviour of host sticklebacks has been extensively tested, and the various changes that have been recorded and their likely physiological basis and consequences for host ecology are discussed in detail.
The Human Leukocyte Antigen (HLA) is a gene complex that encodes important elements of the human immune system. HLA profile is communicated via olfaction and interindividual diversity is assumed to be advantageous for mate choice. Additionally, HLA diversity appears to enhance satisfaction and sexual attraction in existing romantic partnerships. However, whether this effect is transmitted via body odors and whether it results in an attraction towards HLA-dissimilar individuals and/or an avoidance of HLA-similar ones remains unclear. In the present study, we genotyped couples and asked each participant to rate a body odor sample from their Partner and from three strangers of the opposite sex who expressed a similar or dissimilar HLA-B and HLA-C genotype.
We found no statistically significant preference for HLA similarity or dissimilarity in men. Among women, the observed effects differed depending on hormonal contraception status. Like men, women on hormonal contraception did not exhibit significant HLA-related preferences. However, for women not using hormonal contraceptives, odors from HLA-B and HLA-C similar donors were significantly less attractive than those from HLA dissimilar donors, regardless of whether the samples were from a partner or a stranger. Our findings support the hypothesis that HLA similarity is perceived via body odors and that such similarity affects human attraction. This mechanism may serve an evolutionarily adaptive function in preventing prospective offspring from having
decreased immunocompetence, or decreasing the chance of kin mating.
Studies of MHC‐based mate choice in wild populations often test hypotheses on species exhibiting female choice and male‐male competition, which reflects the general prevalence of females as the choosy sex in natural systems. Here we examined mutual mate choice patterns in a small burrow‐nesting seabird, the Leach's storm‐petrel (Oceanodroma leucorhoa), using the Major Histocompatibility Complex (MHC). The life history and ecology of this species is extreme: both partners work together to fledge a single chick during the breeding season, a task that requires regularly traveling hundreds of kilometers to and from foraging grounds over a six to eight‐week provisioning period. Using a five‐year dataset unprecedented for this species (n=1078 adults and 925 chicks), we found a positive relationship between variation in the likelihood of female reproductive success and heterozygosity at Ocle‐DAB2, a MHC class IIB locus. Contrary to previous reports rejecting disassortative mating as a mechanism for maintaining genetic polymorphism in this species, here we show that males make significant disassortative mate choice decisions. Variability in female reproductive success suggests that the most common homozygous females (Ocle‐DAB2*01 / Ocle‐DAB2*01) may be physiologically disadvantaged and, therefore, less preferred as lifelong partners for choosy males. The results from this study support the role of mate choice in maintaining high levels of MHC variability in a wild seabird species, and highlights the need to incorporate a broader ecological framework and sufficient sample sizes into studies of MHC‐based mating patterns in wild populations in general.
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Diversity at the Major Histocompatibility Complex (MHC) is critical to health and fitness, such that MHC genotype may predict an individual′s quality or compatibility as a competitor, ally, or mate. Moreover, because MHC products can influence the components of bodily secretions, an individual′s body odor may signal its MHC and influence partner identification or mate choice. To investigate MHC-based signaling and recipient sensitivity, we test for odor-gene covariance and behavioral discrimination of MHC diversity and pairwise dissimilarity, under the good genes and good fit paradigms, in a strepsirrhine primate, the ring-tailed lemur ( Lemur catta ). First, we coupled genotyping with gas chromatography-mass spectrometry to investigate if diversity of the MHC-DRB gene is signaled by the chemical diversity of lemur genital scent gland secretions. We also assessed if the chemical similarity between individuals correlated with their MHC similarity. Next, we assessed if lemurs discriminated this chemically encoded, genetic information in opposite-sex conspecifics. We found that both sexes signaled overall MHC diversity and pairwise MHC similarity via genital secretions, but in a sex- and season-dependent manner. Additionally, both sexes discriminated absolute and relative MHC-DRB diversity in the genital odors of opposite-sex conspecifics, supporting previous findings that lemur genital odors function as advertisement of genetic quality. In this species, genital odors provide honest information about an individual′s absolute and relative MHC quality. Complementing evidence in humans and Old World monkeys, our results suggest that reliance on scent signals to communicate MHC quality may be important across the primate lineage.
It has been recently suggested that female mate choice, based on sexually selected ornaments, is an important component of social wasps' reproductive biology. The correlates of male ornaments that could be of a female's interest, however, remain to be investigated. Males of the Neotropical paper wasp Polistes simillimus have sexually dimorphic melanin-based black spots on their faces. In this species, male spots work like sexual ornaments, as it has been experimentally demonstrated that females prefer sexual partners with a higher proportion of black pigment on their faces. We have shown that, under laboratory conditions, male sexual ornamentation positively predicts the strength of the melanization immune response and longevity. Therefore, in P. simillimus, melanin-based facial patterns (ornaments) seem to be honest indicators of male quality.
The chemosensory functions of the human nose are underappreciated. Traditional teaching is that the sense of smell detects volatile compounds, which may then allow the identification of substances that may be beneficial or harmful—such as good versus putrefied food. However, increasing evidence from research in other animals suggests that olfaction may serve another and more important purpose, that of mate selection in sexual reproduction; indeed, olfaction may be an essential impetus for evolution.
An individual's body odour is a characteristic that is used to obtain information about conspecifics. However, to our knowledge the role of body odour and the degree of facial symmetry on testosterone changes among men as indicators of possible rivals has not been investigated yet. A group of 113 men were photographed to obtain their degree of facial symmetry, i.e., the small random deviations in facial bilateral traits. They smelled and assessed the odour of men with different grades of facial symmetry, and donated two saliva samples (pre- and post-stimulus sample) to measure the change in their testosterone levels. We found that testosterone levels decreased in symmetrical men who perceived the odour of asymmetrical men. Our results suggest that men could perceive characteristics in other men that are highly valued by women through odour to identify possible rivals, and that the observed decrease in testosterone levels could be related to an inhibition of competitive behaviours.
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This chapter focuses on the importance of ontogeny and early experience in understanding human olfaction. It examines the emergence of the anatomy and function of nasal chemo sensation, including its development in young organisms as they gain sophistication in sensory-motor and cognitive skills. The chapter summarizes adaptive responses to odour exhibited by infants and young children, including newborns, in individual and social contexts. It studies functional onset of nasochemoreception in both animal and human infants. The chapter further considers the adaptive roles of olfaction in the succession of transitions that are typical of mammals, emphasizing the human case. It explains involvement of olfaction in infants' and children's behaviour in affiliative networks within and outside the family. Finally, the chapter assesses the long-term consequences of early exposure to odorants.
This study examined the relationship between the major histocompatibility complex (MHG) genes and mate choice by wild house mice in a controlled laboratory setting in an attempt to understand the mechanisms maintaining natural MHC diversity. Three rearing groups of wild test mice were produced: nonfostered control mice, mice fostered into families of an inbred laboratory mouse strain, and mice fostered into families of a second mouse strain differing genetically from the first only within the MHC region. At maturity test mice were given a choice of two opposite-sex stimulus mice of the two MHC-congenic strains used for fostering. Test mice were scored for several measures of preference including amount of time spent with either stimulus mouse, and ejaculation with a stimulus mouse. Females in mio of three rearing groups spent more time with one MHC type regardless of rearing environment, suggesting that females did not prefer mates dissimilar from family MHC type. Time preferences tended to he: stronger in females than in males. Male test mice ejaculated indiscriminately. Female wild mice mated to ejaculation more often in longer trials, but these matings were still too infrequent to assess preferences. Fostering had little or no effect on MHC-based mate preferences of wild house mice, and no evidence suggested that MHC was used to avoid inbreeding. Wild female mice may still choose mates based on MHC haplotypes (but do not necessarily prefer MHC-dissimilar mates); other cues are probably also used. Based on these results, inbreeding avoidance does not seem a strong mechanism for maintaining natural MHC diversity.
One evolutionary explanation for the success of sexual reproduction assumes that sex is an advantage in the coevolutionary arms race between pathogens and hosts. Accordingly, an important criterion in mate choice and maternal selection thereafter could be the allelic specificity at polymorphic loci involved in parasite-host interactions, e.g. the MHC (major histocompatibility complex). The MHC has been found to influence mate choice and selective abortions in mice and humans. However, it could also influence the fertilization process itself, i.e. (i) the oocyte's choice for the fertilizing sperm, and (ii) the outcome of the second meiotic division after the sperm has entered the egg. We tested both hypotheses in an in vitro fertilization experiment with two inbred mouse strains congenic for their MHC. The genotypes of the resulting blastocysts were determined by polymerase chain reaction. We found nonrandom MHC combinations in the blastocysts which may result from both possible choice mechanisms. The outcome changed significantly over time, indicating that a choice for MHC combinations during fertilization may be influenced by one or several external factors.
The major histocompatibility complex (MHC) is the prime but not exclusive determinant of genetically specific constitutive body odors, termed odortypes, represented strongly in urine of the mouse. Perception of MHC-determined odortypes influences reproductive behavior in the contexts of mate choice and maintenance of early pregnancy, tending to favor the propagation of one MHC type over another. How MHC genotype determines MHC odortype is unknown. One possible explanation is that differential odorants are generated by populations of commensal microorganisms whose composition is somehow geared to MHC diversity. This hypothesis was tested in the Y-maze system in which mice are trained to distinguish the urinary odors of MHC-congenic mice. First, it was shown that mice could readily be trained to distinguish the urines of germfree MHC-congenic mice. Second, it was shown that mice trained to distinguish the urines of conventionally maintained MHC-cogenic mice could as readily distinguish the urines of germfree MHC-congenic mice. These results imply that MHC-determined odortypes do not depend on odorants generated by microorganisms.
We have recently demonstrated strong MHC-based mating preferences in semi-natural populations of Mus (Potts et al., 1991). These preferences are primarily responsible for a 27% deficiency of homozygotes (relative to random mating expectations) observed in nine independent experimental populations. The strength of these preferences is sufficient to explain the majority of MHC genetic diversity found in natural populations of Mus. Here we expand our analysis of the nature of these mating preferences. Although the majority of the MHC-related non-random mating appears to be controlled by females traveling to nearby territories to mate with the resident male, a significant proportion (approximately one quarter) is explained by settlement patterns. MHC-related non-random settlement patterns were primarily due to an excess of settlement pairs that share no MHC haplotypes. Because males may exercise control over which females settle on their territories, this component of MHC non-random mating provides an explanation for the presence of male controlled MHC-based mating preferences found in laboratory studies (Yamazaki et al. 1976; Yamazaki et al. 1978; Yamazaki et al. 1988). The prevalence of studies showing male MHC mating preferences (Beauchamp et al. 1988) has been theoretically troubling due to the expectation that females should be the choosier sex (Partridge, 1988; Nei and Hughes, 1991). A companion paper in this volume (Manning et al.) provides the theory and empirical support for why female MHC mate choice may be diminished or lost during inbreeding.
To determine the influence of genetic and microbiological factors in producing individually unique urine odors, we used a
go/no-go operant task to assess the ability of eight male Long-Evans rats to discriminate between urine odors from the following
pairs of male rats: (1) two outbred Long-Evans rats, (2) individual conventionally housed rats differing genetically only
at the major histocompatibility complex (PVG vs. PVG.R1), (3) individual PVG versus PVG.R1 rats born by cesarean section and
raised in germfree conditions, and (4) conventionally housed, genetically identical individuals of the PVG or PVG.R1 strains.
Discriminable differences were present between the urine odors used in all four tasks. Analysis of the errors to a criterion
of 85% correct discrimination responses revealed different learning patterns in each task. When bacteria were not present
in genetically different rats (Task 3) and when bacteria were present but there were no genetic differences between rats (Task
4), the discrimination was the most difficult. The easiest discrimination involved the presence of bacteria and a genetic
difference at the major histocompatibility complex (Task 2). These results indicate that, although bacteria are not necessary
for the production of discriminable odor differences, they do influence the discriminability of the urine odors of rats.
Olfactory information is critical to mammalian sexual behavior. Based on parental investment theory the relative importance
of olfaction compared with vision, touch, and hearing should be different for human males and females. In particular, because
of its link to immunological profile and offspring viability, odor should be a more important determinant of sexual choice
and arousal for females than for males. To test this hypothesis a questionnaire was developed and administered to 332 adults
(166 males, 166 females). Subjects used a 1–7 scale to indicate how much they agreed with a series of statements concerning
the importance of olfactory, visual, auditory, and tactile information for their sexual responsivity. The data reveal that
males rated visual and olfactory information as being equally important for selecting a lover, while females considered olfactory
information to be the single most important variable in mate choice. Additionally, when considering sexual activity, females
singled out body odor from all other sensory experiences as most able to negatively affect desire, while males regarded odors
as much more neutral stimuli for sexual arousal. The present results support recent findings in mice and humans concerning
the relation of female preferences in body odor and major histocompatibility complex (MHC) compatibility and can be explained
by an evolutionary analysis of sex differences in reproductive strategies. This work represents the first direct examination
of the role of different forms of sensory information in human sexual behavior.
When a male mouse is presented with two H-2 congenic two female in estrus, his choice of a mate is influenced by their H-2 types. The term "strain preference" is used to describe the general tendency of the male population of one inbred strain to prefer two female of one H-2 type rather than another. The term "consistency of choice" is used to describe the added tendency of particular two males of one inbred strain, in sequential mating trials, to prefer two females of the H-2 type they chose in previous trials. Statistical analysis showed trends in the data that support the following conclusions: (a) The choice is made by the male, not the female. (b) The strain preference of two males may favor two females of dissimilar H-2 type (four of six comparisons), or of similar H-2 type (one of six comparisons). (c) Consistency of choice does not always correspond with strain preference. In one of six comparisons of H-2 genotypes there was no strain preference but pronounced consistency of choice by individual two male. This suggests memory, but fortuitous bias is not excluded. (d) Strain preference of the same male population may favor two male of the same or a different H-2 type, depending on which different H-2 type is offered as the choice alternative to self. These findings conform to a provisional model in which olfactory mating preference is governed by two linked genes in the region of H-2, one for the female signal and one for the male receptor. These mating preferences could in natural populations serve the purpose of increasing the representation of particular H-2 haplotypes or of maintaining heterozygosity of genes in the region of H-2.
House mice (Mus musculus domesticus) form communal nests and appear to nurse each other's pups indiscriminately. Communal nesting probably functions to reduce infanticide, but it also makes females vulnerable to exploitation if nursing partners fail to provide their fair share of care. Kinship theory predicts that females will preferentially form communal nests with relatives to minimize exploitation and further increase inclusive fitness. Here we provide evidence from seminatural populations that females prefer communal nesting partners that share allelic forms of major histocompatibility complex genes. Such behaviour would lead to the selection of close relatives as communal nesting partners. Although criteria for the demonstration of kin recognition are currently embroiled in controversy, this is the first vertebrate study to meet Grafen's restrictive requirements: discrimination is based on genetic similarity at highly polymorphic loci, incidental correlations due to relatedness are experimentally controlled, and strong reasons exist for expecting the assayed behaviour to be kin-selected.
The extended H-2 complex of genes in the mouse includes at least three loci that independently specify distinctive body odors, "odortypes," whose differential recognition influences mating choice and affects the maintenance of early pregnancy. A prime experimental method of identifying H-2 odortypes is the specially designed Y-maze in which mice are trained, by water deprivation and reward, to distinguish odors conducted to the arms of the maze from H-2-dissimilar mice or their urines. It is confirmed that H-2-dissimilar infant mice, unlike adult mice, are not distinguished by trained mice in the Y-maze. However, a previous conclusion that infant mice do not express H-2 odortypes is shown to be incorrect, because the urines of H-2-dissimilar infant mice, even at 1 day of age, were distinguished in the Y-maze. Thus urine, ingested by the mother, clearly could suffice for her to distinguish her own from other H-2-dissimilar pups. Further, urine would seem to be a unique source of H-2 odortypes. If, as we believe, H-2 odortypes represent mostly compound odors composed by H-2 genetic variation in the urinary output of odorous metabolites, as distinct from simple odors that depend on chemical differences of single odorants, then the kidney, which is not responsible for H-2 odortype specificity, may nevertheless impart a unique character to urinary odortypes by virtue of differential excretion/resorption processing of various constituent odorous metabolites. In that case, various organs and tissues, among which the hematopoietic/lymphoid system is known to contribute to H-2 odortype specificity, may exhibit tissue-specific varieties of H-2 odortypes, their products having not yet been subjected to renal processing.
Genetic polymorphism in the H-2:Qa:Tla region of chromosome 17 is associated with constitutive variation of bodily odor phenotypes which permit individual olfactory recognition among mice (Boyse et al.1987). We previously found that differences in the MHC genes affect the mating choices of mice (Yamazaki et al. 1976, 1978, 1988; Andrews and Boyse, 1978; Yamaguchi et al., 1978), and that mice can be trained to distinguish arms of a Y-maze scented by odors from mice differing only in this genetic region (Yamazaki et al.,1979, 1982; Yamaguchi et al.,1981). We also showed a raised incidence of blockage of pregnancy or pseudopregnancy in mated females exposed to the scent of alien males whose MHC type differs from that of the mate (Yamazaki et al., 1983). As no known gene complex exhibits such vast diversity as the MHC, its potential as a major source for genetically based signals of individual identity is great.
Classical class I transplantation antigens (HLA-A, -B, -C in man; H-2K, H-2D in mouse) of the major histocompatibility complex (MHC) are membrane-bound glycoproteins that act as restricting elements in antigen recognition by T-lymphocytes (Klein 1986). However, there have been reports of classical class I transplantation antigens that have been found in true solution in the body fluids of mouse (Callahan et al. 1975, 1976), man (van Rood et al. 1970; Vincent and Revillard 1979), and rat (Spencer and Fabre 1987; Singh et al. 1987a). The function of these molecules has not been defined but suggestions ranging from there being no function for them at all (Gussow and Ploegh 1987) to a role for them in inducing tolerance to self (Kamada et al. 1981; Kress et al. 1983; Cosman et al. 1982) have been put forward.
The Major Histocompatibility Complex (MHC) appears to provide the genetic basis for an individuality marker in the urine of rats and mice (Brown, Singh and Roser, 1987; Brown, Roser and Singh, 1990; Yamazaki et al., 1991). Recent findings suggest that commensal bacteria are also involved in the production of individually distinct urine odors in rats. Using a habituation-dishabituation task, Singh et al. (1990) determined that rats could not discriminate between the urine of germfree MHC congenic rats (PVG vs. PVG.R1). When donors were moved to conventional housing, their urines could be discriminated. Also, rats trained in a go-no go operant task in an olfactometer made more errors in learning to discriminate between urines of germfree MHC congenic rats than between urines of conventionally housed MHC congenic rats (Schellinck, Brown and Slotnick, 1991). Urine odors from conventionally housed MHC congenic rats were readily discriminated; the discrimination was remembered from session to session and no drop in performance was observed when the samples were changed to different donors of the same MHC type in midsession. Although the rats were able to discriminate between urine samples from individual germfree MHC congenic rats, they consistently performed at chance at the beginning of each session. One explanation of this inability to retain the information from session to session could be that constant cues were not being used to discriminate between the urine samples from germfree rats. Moreover, when the urine samples from germfree rats were changed to others of the same strain in midsession, performance was also disrupted.
Amongst its many odour signals, urine emits an odour, unique to each individual, which is directly related to the MHC type (Yamazaki et al., 1976, Singh et al., 1987, Brown et al., 1989). Extreme polymorphism of the class I MHC loci provides sufficient variation within a species to confer uniqueness on individuals at this molecular level (Klein, 1982). However, the way in which this protein polymorphism is expressed as odour polymorphism in the urine is not known. Since the MHC class I molecules are themselves excreted in the urine, they could be thought to provide individually unique signals except that they are non-volatile proteins and therefore not detectable by smell. Because the excreted class I molecules are extensively degraded in the urine (Singh et al., 1987), it is possible that aromatic amino acids, characteristic of the variable sequences in the heavy chain contribute the aromatic signals. However, since most amino acids have no smell, this explanation seems unlikely.
Odortypes, defined as genetically-determined body odors that enable individuals of a species to distinguish one another by odor, are specified in part by polymorphic genes of the Major Histocompatibility Complex or MHC. The participation of the MHC in individual odor constitution may shed light on evolutionary and developmental functions of the MHC (Beauchamp et al., 1986; Boyse et al., 1987, 1991; Yamazaki et al., 1991). These functions have long been suspected to account for many non-immunological correlates of MHC polymorphism which have no obvious connection with the precisely defined immunological functions of the MHC (review in Boyse et al., 1983), but which may signify more rudimentary functions that preceded the specific adaptive immunity which is fully manifested only in vertebrates.
Up to now, MHC-related odors have been only described for rodents Yamazaki et al., 1991; Roser et al., 1991). Nevertheless, it has been speculated that a similar phenomenon may also occur in humans (Beauchamp et al., 1985; Boyse et al., 1987). Individual specific body odors do indeed play a role in human self-perception (Porter and Moore, 1981; Lord and Kasprzak, 1989) and recognition of offspring (Porter et al., 1983; Kaitz et al., 1987), but there is no information available on the biological basis of these odors.
Previous studies of mating preference signified that mice can sense one another's major histocompatibility complex (MHC) types, probably by olfaction. This conclusion has now been substantiated by the use of a Y-maze whose two arms were differentially scented with currents of air conducted through boxes occupied by B6 (H-2b) males and by B6-H-2k congenic males. Four B6 mice, two males and two females, were successfully trained, by water deprivation and reward, to enter the arm scented by B6 or B6-H-2k males. One of the males and one of the females were trained to select the B6-scented arm; the other male and female were trained to select the B6-H-2k-scented arm. Untrained mice showed no MHC discrimination in the maze. The performance of the trained mice in distinguishing between MHC congenic homozygous F2 segregants derived from a cross of B6-H-2k with B6 was as good as their performance in distinguishing the respective inbred strains, thus essentially eliminating alternative and significant additional explanations of MHC-associated sensory discrimination. The data further indicate that chemosensory discrimination of MHC types can be entirely dissociated from sex differences and from the circumstances of mating.
Classical class I transplantation antigens present in solution in the body fluids have been studied. These antigens have been found in a monomeric, soluble form in blood, lymph, and urine, and a major source is the hemopoietic system which gives rise to cells that secrete these molecules into the blood. The cell types most probably involved in their secretion are of the macrophage/dendritic cell lineage. The serum molecule is a heterodimer with a heavy chain of 39,000 mol wt associated noncovalently with beta 2-microglobulin and is present in serum at a concentration between 350 and 390 ng/ml. These molecules have a short half-life of 2.7 h and are excreted into the environment via the kidneys in the urine. In the urine, greater than 90% of the molecules are degraded into smaller fragments. This finding that normal metabolic processes lead to the excretion of classical highly polymorphic class I molecules in the urine provides a direct explanation in molecular terms of the ability of animals to identify individuals on the basis of urinary odor. Since intact class I molecules are unlikely to be the odoriferous component in the urine, two hypotheses have been suggested. Either small fragments of class I molecules are detected or the molecule acts as a carrier that transports volatiles from the serum into the urine where they are released, giving rise to the class I-associated odor.
When a male mouse is presented with two H-2 congenic two female in estrus, his choice of a mate is influenced by their H-2 types. The term "strain preference" is used to describe the general tendency of the male population of one inbred strain to prefer two female of one H-2 type rather than another. The term "consistency of choice" is used to describe the added tendency of particular two males of one inbred strain, in sequential mating trials, to prefer two females of the H-2 type they chose in previous trials. Statistical analysis showed trends in the data that support the following conclusions: (a) The choice is made by the male, not the female. (b) The strain preference of two males may favor two females of dissimilar H-2 type (four of six comparisons), or of similar H-2 type (one of six comparisons). (c) Consistency of choice does not always correspond with strain preference. In one of six comparisons of H-2 genotypes there was no strain preference but pronounced consistency of choice by individual two male.This suggests memory, but fortuitous bias is not excluded. (d) Strain preference of the same male population may favor two male of the same or a different H-2 type, depending on which different H-2 type is offered as the choice alternative to self.These findings conform to a provisional model in which olfactory mating preference is governed by two linked genes in the region of H-2, one for the female signal and one for the male receptor. These mating preferences could in natural populations serve the purpose of increasing the representation of particular H-2 haplotypes or of maintaining heterozygosity of genes in the region of H-2.
Radiation chimeras were made by restoring lethally irradiated inbred mice with bone marrow cells of F1 hybrid mice of crosses between that inbred strain and an H-2-congenic strain. The urine of these chimeras was tested by the Y maze method, and shown to have acquired a scent indicative of the reconstituting donors' H-2 type. Thus, cells of the hematopoietic system contribute to the H-2-related odorant properties that enable mice to distinguish one another according to their H-2 types.
High-resolution chromatographic profiles of urinary volatiles were quantitatively recorded and statistically evaluated for the female mice genetically differing in a small region of the major histocompatibility complex on the 17th chromosome. Both immature and estrogenized animals were evaluated. While there seem to be no specific volatile products of the histocompatibility genes, statistically significant differences were readily observed with the immature females of different haplotypes, involving the general range of secondary volatile metabolites. Their possible role in olfactory communication is discussed.
In order to test the hypothesis that commensal bacteria influence the urinary odors of individuality, we collected urine from PVG and PVG.R1 male rats born by cesarian section and reared in a germ-free environment. Using the habituation-dishabituation test with PVG.RT1
u
and Lister hooded rats as subjects, we found that urine from the germ-free rats was not discriminated, while urine from conventionally housed rats of the same strains could be discriminated (experiment 1). When the germ-free rats were moved to a conventional animal house after recolonization with commensural flora and their urine collected, it was discriminated, indicating an essential role of bacteria in determining the unique urinary odors of MHC-congenic rats (experiment 2). The conventionally housed and germ-free rats did not differ in the amount of class I antigen in their urine (experiment 3). Finally, urines of PVG and PVG.R1 donors inoculated with a defined and highly restricted flora to render them specific-pathogen-free (SPF) could not be discriminated. Urine from SPF donors moved to a conventional animal house could be discriminated (experiment 4). These results indicate that commensal bacteria are essential for the production of the unique individual odor of the urine of MHC-congenic strains of rats.
Mice can discriminate samples of urine obtained from two groups of inbred mice that are genetically identical except in their major histocompatibility complex (MHC) haplotype (congenic mice), whereas they cannot distinguish urine samples from two genetically identical groups of mice. Chemical fractions of urine samples obtained from MHC congenic mice were tested in a Y-maze olfactometer using a method modified to accommodate the bioassay to chemical fractions that might differ in sensory properties from the unfractionated urine. Fractions depleted in protein by several methods were consistently discriminable by mice in the Y maze, providing a direct demonstration that the airborne MHC genotype information can be conveyed by volatile compounds alone.
Genes of the highly polymorphic H-2 major histocompatibility complex impart to each mouse a scent that is characteristic of its H-2 haplotype. Recognition of these individual odors affects mate choice and other aspects of reproduction. Other parts of the genome also contribute to genetically determined individuality of body scent.
This chapter discusses the behavior and major histocompatibility complex (MHC) of the mouse. The MHC provides each mouse with a characteristic odor, called an odor type, which is indicative of its MHC genotype. The rest of the autosomal genome, and each sex chromosome, determine independent odortypes. This chapter describes the following three elements of social intercourse: (1) the message, (2) reception of the message, and (3) response to the message. The usual tendency of inbred males to mate with females of a different MHC type is because of familial imprinting in early life and, thus, can be reversed by neonatal transfer to foster parents whose MHC type differs from that of the male. Responses of relevance to reproduction are seen also in females. Thus, termination of early pregnancy is much more frequent among isolated females that sense a male MHC odortype different from that of the missing stud male.
Commentary on a research paper reporting that a male mouse will tend to pick a female mouse to impregnate on the basis of the alleles she carries in her histocompatibility (H-2) system thus suggesting a possible link between histocompatibility antigens and pheromones is presented. Further clarification of just how these results occur is suggested. These H-2-associated matings would encourage polymorphism. Heterozygous advantages in H-2 have been demonstrated with regard to viral antigens on cell surfaces. Recognition of genetically endowed polymorphic pheromones could also play a part in maintaining the genetic integrity of incipient species in the face of constant risk of interbreeding with the parent species. Further research in this area is suggested.
It has been convincingly demonstrated that mice can discriminate MHC-related odors among congenic strains under laboratory conditions (see Yamaguchi et al. 1981). There is, however, debate about the use of these MHC-related odors as mate choice cues (Partridge, 1988; Klein et al., 1990; Nei and Hughes, 1991). MHC-based mate choice has been postulated to function either to produce presumably more fit MHC heterozygous offspring (Doherty and Zinkernagel, 1975) or to avoid close inbreeding (Brown, 1983). In either case, mating should be disassortative. Data from semi-natural half-wild enclosure studies (Potts et al., 1991) suggest that disassortative matings produce an excess (from random mating expectations) of MHC heterozygous progeny. Behavioral observations also suggest that these disassortative matings are due primarily to female choice. In a subset of 305 pups of known maternity, those in litters of mixed paternity (30 out of 58 litters) show a significant excess of heterozygotes over what would have been produced if females had mated only with their territorial males. Those litters sired only by the female’s territorial male did not deviate from the number of heterozygotes expected. This suggests that an important factor in producing more MHC heterozygous progeny is extra-territorial matings. In 41 observations of mating pairs, all matings took place on the territory of the male. All 13 extra-pair matings observed involved females who had left their nesting territory to travel to the territory of the male with which they were mating. No male was ever observed mating off of his territory. For details see Potts et al. this volume.
Tested male mice with female odors from soiled bedding and with tethered females to compare the mate and odor preferences of males and females of the same 2 congenic strains, C57BL/10Sn.CHR51 (CHR) and C57BL/10Sn.GAA37 (GAA). Males showed no preference for the odors of females of either major histocompatibility complex (MHC) strain. In the mate-choice experiment, males also showed no preference for females of either haplotype. Although males of both the strains did not exhibit a mate preference with respect to female MHC-haplotype, males of the 2 strains differed in the probability that they would mate. CHR males were more likely than GAA males to ejaculate with a test female. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Male and female F2 homozygotes from crosses between MHC-congenic inbred mouse strains were tested for MHC-associated mating preference. In three instances, of the four genotypic combinations so tested, marked MHC-associated mating preference was observed. This result greatly reduces the possibility that the observed mating preferences of MHC-congenic inbred strains can be explained wholly in terms of non-MHC genetic drift, or of residual non-MHC genetic disparity, or of fortuitous acquired strain characteristics unrelated to MHC. In two of the four combinations investigated, the MHC-related mating bias of F2 segregants was similar to that of the genotypically similar inbred parent strains. In a third combination, F2 segregants did not show the mating bias exhibited by the corresponding parent strains. In a fourth combination, F2 segregants displayed an MHC-related mating bias that was evident in the corresponding parental inbred strains only when the colonies of the parent strains had been maintained in isolation from other strains. While the exhibition of mating preference by mice of the same genotypes may differ according to circumstances, as indicated, in no instance was preference reversed. Mating preference in a given combination of MHC genotypes, whenever it was observed, always favored the same MHC haplotype of the two alternative haplotypes represented. It appears that the familial MHC genotypes of mice and the environment in which the colonies are maintained influence their MHC-related mating preference, but it has yet to be decided whether these factors operate by determining exposure to particular MHC haplotypes.
Species recognition and group member recognition systems produce an ability to discriminate conspecifics by genetic similarity on first encounter when kin recognition is absent. Experimental evidence of such discrimination is therefore insufficient evidence for kin recognition. The evolution of a true kin recognition system depends on three kinds of loci: matching, detection and using. Matching loci, which affect the traits used to detect kin, will have a higher genetic similarity between interactants than their common ancestry alone suggests. Selection has been erroneously thought to cause individuals to behave according to the higher relatedness implied by this extra similarity. The detection loci and using loci are not expected to be closely linked to the matching loci, implying that individuals will behave according to the relatedness based on their common ancestry. Polymorphism at the matching loci is essential for effective discrimination of kin, and is sustained by the evolution of the kin recognition system in those cases where it is advantageous to interact with kin.
Male mice of the LACA strain and from a wild stock were allowed to form territories in 180-cm2 enclosures. The clues by which they recognized the position of the territory boundaries were investigated by moving various landmarks or reference objects. The information used was found to be primarily visual, close objects taking precedence over distant ones. Olfactory clues were also used but only when they did not conflict with the visual ones. Cover was found to be necessary for territory formation, but not for maintenance, and the size of the territory apparently influenced the aggressiveness of the mouse holding it.
The murine major histocompatibility complex (MHC) includes sequences that are responsible for haplotype-specific odor types that, in turn, influence mating preference. We report that there are several olfactory receptor genes or pseudogenes in the Class I region of the human MHC. At least one of these genes is intact, appears to encode an mRNA, and is quite homologous to a previously reported murine olfactory receptor.
Selection clearly focuses on differences in reproduction, but studies of reproductive physiology generally have been carried out in a near vacuum of modern evolutionary theory. This lack of contact between the two fields may be about to change. New ideas indicate that sexual selection by cryptic female choice has affected the evolution of products in male semen that influence female reproductive behavior and physiology.