Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs)
Abstract Background Reliable recognition of individuals requires phenotypic identity signatures that are both individually distinctive and appropriately stable over time. Individual-specific vocalisations or visual patterning are well documented among birds and some mammals, whilst odours play a key...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2018-04-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12915-018-0512-9 |
| _version_ | 1818596278334914560 |
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| author | Sarah A. Roberts Mark C. Prescott Amanda J. Davidson Lynn McLean Robert J. Beynon Jane L. Hurst |
| author_facet | Sarah A. Roberts Mark C. Prescott Amanda J. Davidson Lynn McLean Robert J. Beynon Jane L. Hurst |
| author_sort | Sarah A. Roberts |
| collection | DOAJ |
| description | Abstract Background Reliable recognition of individuals requires phenotypic identity signatures that are both individually distinctive and appropriately stable over time. Individual-specific vocalisations or visual patterning are well documented among birds and some mammals, whilst odours play a key role in social recognition across many vertebrates and invertebrates. Less well understood, though, is whether individuals are recognised through variation in cues that arise incidentally from a wide variety of genetic and non-genetic differences between individuals, or whether animals evolve distinctive polymorphic signals to advertise identity reliably. As a bioassay to understand the derivation of individual-specific odour signatures, we use female attraction to the individual odours of male house mice (Mus musculus domesticus), learned on contact with a male’s scent marks. Results Learned volatile odour signatures are determined predominantly by individual differences in involatile major urinary protein (MUP) signatures, a specialised set of communication proteins that mice secrete in their urine. Recognition of odour signatures in genetically distinct mice depended on differences in individual MUP genotype. Direct manipulation using recombinant MUPs confirmed predictable changes in volatile signature recognition according to the degree of matching between MUP profiles and the learned urine template. Both the relative amount of the male-specific MUP pheromone darcin, which induces odour learning, and other MUP isoforms influenced learned odour signatures. By contrast, odour recognition was not significantly influenced by individual major histocompatibility complex genotype. MUP profiles shape volatile odour signatures through isoform-specific differences in binding and release of urinary volatiles from scent deposits, such that volatile signatures were recognised from the urinary protein fraction alone. Manipulation using recombinant MUPs led to quantitative changes in the release of known MUP ligands from scent deposits, with MUP-specific and volatile-specific effects. Conclusions Despite assumptions that many genes contribute to odours that can be used to recognise individuals, mice have evolved a polymorphic combinatorial MUP signature that shapes distinctive volatile signatures in their scent. Such specific signals may be more prevalent within complex body odours than previously realised, contributing to the evolution of phenotypic diversity within species. However, differences in selection may also result in species-specific constraints on the ability to recognise individuals through complex body scents. |
| first_indexed | 2024-12-16T11:29:22Z |
| format | Article |
| id | doaj.art-ab203fd414b2418282221bbb4b7c83e3 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-16T11:29:22Z |
| publishDate | 2018-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-ab203fd414b2418282221bbb4b7c83e32022-12-21T22:33:17ZengBMCBMC Biology1741-70072018-04-0116111910.1186/s12915-018-0512-9Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs)Sarah A. Roberts0Mark C. Prescott1Amanda J. Davidson2Lynn McLean3Robert J. Beynon4Jane L. Hurst5Mammalian Behaviour & Evolution Group, Institute of Integrative Biology, University of LiverpoolCentre for Proteome Research, Institute of Integrative Biology, University of LiverpoolMammalian Behaviour & Evolution Group, Institute of Integrative Biology, University of LiverpoolCentre for Proteome Research, Institute of Integrative Biology, University of LiverpoolCentre for Proteome Research, Institute of Integrative Biology, University of LiverpoolMammalian Behaviour & Evolution Group, Institute of Integrative Biology, University of LiverpoolAbstract Background Reliable recognition of individuals requires phenotypic identity signatures that are both individually distinctive and appropriately stable over time. Individual-specific vocalisations or visual patterning are well documented among birds and some mammals, whilst odours play a key role in social recognition across many vertebrates and invertebrates. Less well understood, though, is whether individuals are recognised through variation in cues that arise incidentally from a wide variety of genetic and non-genetic differences between individuals, or whether animals evolve distinctive polymorphic signals to advertise identity reliably. As a bioassay to understand the derivation of individual-specific odour signatures, we use female attraction to the individual odours of male house mice (Mus musculus domesticus), learned on contact with a male’s scent marks. Results Learned volatile odour signatures are determined predominantly by individual differences in involatile major urinary protein (MUP) signatures, a specialised set of communication proteins that mice secrete in their urine. Recognition of odour signatures in genetically distinct mice depended on differences in individual MUP genotype. Direct manipulation using recombinant MUPs confirmed predictable changes in volatile signature recognition according to the degree of matching between MUP profiles and the learned urine template. Both the relative amount of the male-specific MUP pheromone darcin, which induces odour learning, and other MUP isoforms influenced learned odour signatures. By contrast, odour recognition was not significantly influenced by individual major histocompatibility complex genotype. MUP profiles shape volatile odour signatures through isoform-specific differences in binding and release of urinary volatiles from scent deposits, such that volatile signatures were recognised from the urinary protein fraction alone. Manipulation using recombinant MUPs led to quantitative changes in the release of known MUP ligands from scent deposits, with MUP-specific and volatile-specific effects. Conclusions Despite assumptions that many genes contribute to odours that can be used to recognise individuals, mice have evolved a polymorphic combinatorial MUP signature that shapes distinctive volatile signatures in their scent. Such specific signals may be more prevalent within complex body odours than previously realised, contributing to the evolution of phenotypic diversity within species. However, differences in selection may also result in species-specific constraints on the ability to recognise individuals through complex body scents.http://link.springer.com/article/10.1186/s12915-018-0512-9Individual recognitionOlfactory communicationCommunication signalsSignature mixturesPheromonesHouse mice |
| spellingShingle | Sarah A. Roberts Mark C. Prescott Amanda J. Davidson Lynn McLean Robert J. Beynon Jane L. Hurst Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs) BMC Biology Individual recognition Olfactory communication Communication signals Signature mixtures Pheromones House mice |
| title | Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs) |
| title_full | Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs) |
| title_fullStr | Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs) |
| title_full_unstemmed | Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs) |
| title_short | Individual odour signatures that mice learn are shaped by involatile major urinary proteins (MUPs) |
| title_sort | individual odour signatures that mice learn are shaped by involatile major urinary proteins mups |
| topic | Individual recognition Olfactory communication Communication signals Signature mixtures Pheromones House mice |
| url | http://link.springer.com/article/10.1186/s12915-018-0512-9 |
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