T
he thesis ofthis chapter is that sexual selection
(usually male-male competition and female choice)
operating in captive house mouse societies can be
exploited to examine fitness components of genes (or other
manipulated variables) that are critical for success in the
wild. Since sexual selection can be studied in seminatural
populations of Mus,we have used this simplified approach
to reveal major fitness differences that were largely invisible
when studying the animals with traditional laboratory ap-
proaches. The model-organism status of the house mouse
provides the opportunity to merge the powerful approaches
of molecular, cell, and physiological biology with the tools
of field ecology. We hope our attempt to fuse these different
levels of analysis in the house mouse serves as a model for
developing such integrative approaches for the biological
study of other social species.
There are recent compelling examples in animals, includ-
ing rodents, that both intra- and intersexual selection favor
mates with “good genes” and consequently produce off-
spring with higher fitness (Møller and Alatalo 1999; Drick-
amer et al. 2000; Calsbeek and Sinervo 2002; Hine et al.
2002; Drickamer et al. 2003; Gowaty et al. 2003). The ulti-
mate measure of fitness is lifetime reproductive success, and
since the most robust, pathogen-free, predator-savvy ani-
mals are those that survive to breed, mice compete for habi-
tats that have predator-free hiding sites, and they compete
for habitat with the best food resources. For this reason,
in social species with intrasexual competition, sexual selec-
tion likely produces fitness outcomes approximating those
of natural selection, even in seminatural population studies
lacking many of the important components of natural se-
lection. In nature, the losers of intrasexual competition are
killed by starvation, predators, and disease. In our system,
such animals do not breed because they are excluded from
territories by competitors, and fail to gain access to mates.
Fitness measures have always been critical to questions in
ecology and evolution, but increasingly they are needed to
answer questions in molecular disciplines, where genes are
experimentally manipulated to assay function. Perhaps the
foremost category of molecular questions requiring fitness
measures is in the field of functional genomics. As functional
genomics programs begin to discover the power of fitness
assays for revealing phenotypes, we expect such methodol-
ogies to become incorporated into the functional genomics
toolbox. Conversely, insight into compelling problems at
the ecological level can be gained by illuminating the mech-
anistic underpinnings of gene function. Reductionist scien-
tists have committed what might be considered the ultimate
reductionist act — the complete sequencing of genomes.
Now we must find out what those genes do, from molecule
to cell to organ to organismal fitness —what is their func-
tion in nature?
In the following pages, we relay the stories of three evo-
lutionary puzzles that are also the stories of three natural
genetic experiments whose corresponding phenotypes were
either invisible or insufficiently resolved using laboratory
approaches. The solution to each puzzle came only after re-
lease from the restrictive confines of the laboratory into the
rich and informative context of Mussocial structure. First,
we review the role of the major histocompatibility complex
(MHC) in mate choice and discuss evidence that sexual se-
lection helps maintain the tremendous polymorphisms at