genetically-based olfactory signatures persist despite dietary variations

Eugen Leitl eugen at
Fri Nov 14 04:52:19 PST 2008

Genetically-Based Olfactory Signatures Persist Despite Dietary Variation

Jae Kwak1, Alan Willse2B$a, Koichi Matsumura1, Maryanne Curran Opiekun1,
Weiguang Yi1B$b, George Preti1,3, Kunio Yamazaki1, Gary K. Beauchamp1*

1 Monell Chemical Senses Center, Philadelphia, Pennsylvania, United States of
America, 2 Battelle - Pacific Northwest Division, Richland, Washington,
United States of America, 3 Department of Dermatology, School of Medicine,
University of Pennsylvania, Philadelphia, Pennsylvania, United States of
America Abstract

Individual mice have a unique odor, or odortype, that facilitates individual
recognition. Odortypes, like other phenotypes, can be influenced by genetic
and environmental variation. The genetic influence derives in part from genes
of the major histocompatibility complex (MHC). A major environmental
influence is diet, which could obscure the genetic contribution to odortype.
Because odortype stability is a prerequisite for individual recognition under
normal behavioral conditions, we investigated whether MHC-determined urinary
odortypes of inbred mice can be identified in the face of large diet-induced
variation. Mice trained to discriminate urines from panels of mice that
differed both in diet and MHC type found the diet odor more salient in
generalization trials. Nevertheless, when mice were trained to discriminate
mice with only MHC differences (but on the same diet), they recognized the
MHC difference when tested with urines from mice on a different diet. This
indicates that MHC odor profiles remain despite large dietary variation.
Chemical analyses of urinary volatile organic compounds (VOCs) extracted by
solid phase microextraction (SPME) and analyzed by gas chromatography/mass
spectrometry (GC/MS) are consistent with this inference. Although diet
influenced VOC variation more than MHC, with algorithmic training (supervised
classification) MHC types could be accurately discriminated across different
diets. Thus, although there are clear diet effects on urinary volatile
profiles, they do not obscure MHC effects.

Citation: Kwak J, Willse A, Matsumura K, Curran Opiekun M, Yi W, et al.
(2008) Genetically-Based Olfactory Signatures Persist Despite Dietary
Variation. PLoS ONE 3(10): e3591. doi:10.1371/journal.pone.0003591

Editor: Hiroaki Matsunami, Duke Unviersity, United States of America

Received: April 21, 2008; Accepted: September 26, 2008; Published: October
31, 2008

Copyright: B) 2008 Kwak et al. This is an open-access article distributed
under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited.

Funding: This work is supported by ARO contract DAAD19-03-1-0109. Opinions,
interpretations, conclusions, and recommendations are those of the authors
and are not necessarily endorsed by the United States Government.

Competing interests: The authors have declared that no competing interests

* E-mail: beauchamp at

B$a Current address: Monsanto Company, Ankeny, Iowa, United States of America

B$b Current address: Department of Horticulture, University of Georgia,
Athens, Georgia, United States of America Introduction

For social animals, an ability to identify individuals is almost a
prerequisite for the efficient organization of behavioral interactions. Many
studies have demonstrated that individual animals can recognize one another
as individuals and that, for mammals in particular, body volatiles (herein
referred to loosely as odors) detected by olfactory or vomeronasal receptors
play a prominent role in mediating this individual recognition [1]. We have
previously proposed that each individual mouse has a unique odor which we
have termed its odortype [2]. Odortypes, like other phenotypes, are
influenced by genetic and environmental variation, and possibly their
interaction. Among the genetic bases for individual odortypes, variation in
genes of the MHC plays a central role as we and many others have demonstrated
[2]b[5]. Variation in non-MHC genes can also influence the urinary odors of
mice and contribute toward specification of genetically-determined odortypes

Individual identity, as it is commonly conceived, is the sum of the
characteristics of an individual animal that distinguish it from other
members of its species. It is generally assumed that these individual
characteristics must be relatively stable over considerable time periods so
that the individual can be recognized in multiple behavioral and social
contexts. Thus for odortypes it would seem desirable that they be stable over
time and relatively uninfluenced by day-to-day fluctuations due to such
factors as variation in diet.

Nevertheless, there is considerable evidence suggesting short-term
fluctuations in body odors due to variation in stress [9], disease state
[10], [11] and diet [12], [13 and reference therein]. Some reports suggest
that dietary changes might mask genetically determined odortypes, preventing
individual recognition [14], [15]. However, it would be surprising if an
altered diet made it impossible to recognize genetically-determined
individuality of odor, as Schellinck et al [15] suggest. Instead, we
hypothesize that genetically-determined odortypes, and particularly
MHC-determined odortypes, are relatively buffered against changes due to
short-term environmental fluctuations. Such buffering would seem to be a
prerequisite for MHC odortypes to be involved in mediating mate choice in
natural environments, as studies in semi-natural testing conditions suggest

To clarify the influence of diet on MHC-regulated odortypes, we conducted
combined behavioral and chemical studies using urine samples from two
different congenic mouse strains each on two different diets. First, we
tested whether MHC odortypes are perceived following substantial changes in
diet. We found that although diet clearly has a large effect on urinary
odors, MHC-determined odortype variation can be recognized in spite of major
diet variation. Chemical analyses of urinary VOCs for these same mice were
completely consistent with behavioral results: dietary variation
significantly altered the profile of urinary VOCs, but a clear subset of MHC
determined VOCs was unperturbed by diet variation, allowing for statistical
discrimination of MHC types across dietary treatments.


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