giant jumping rat (Hypogeomys antimena) is strictly mo-
nogamous, has low MHC polymorphisms, low reproduc-
tive rates, and restricted gene flow (Sommer et al. 2002).
The authors found a similar pattern of monogamy and low
MHC diversity in another monogamous Malagasy rodent
species, but nearly double the MHC polymorphisms in a
third species with a promiscuous mating system, suggest-
ing a correlation between type of mating system and MHC
diversity. Interestingly, variation in geographic distribution
did not account for variation in MHC polymorphisms
among these three sympatric species (Sommer et al. 2002).
Social structure may similarly influence MHC diversity of
Argentine tuco-tucos (Ctenomys), where balancing selec-
tion for MHC Class II DQ was found to be enhanced in a
social species compared to a solitary species (Hambuch and
Lacey 2002). It is not clear why monogamy or solitary so-
cial structure should reduce balancing selection on MHC
loci. However, even if MHC-based mating preferences are
active in these systems, low polymorphism might be an un-
avoidable consequence of reduced gene flow increasing the
effect of drift, as is found on island populations of the Aus-
tralian bush rat (Seddon and Baverstock 1999). It would
be worthwhile to examine the possibility that the social
ecology of such rodents reduces their parasite loads, which
could serve to counterbalance the loss of MHC diversity.
As MHC diversity increases in populations, so does
the statistical difficulty of analyzing those populations for
MHC-based mating preferences. The more alleles that are
available to choose from, the more likely it is that ani-
mals will pair with MHC-dissimilar individuals by chance
alone, requiring excessive power to detect statistical signifi-
cance. This may be why MHC-based mating preferences
have rarely been detected in wild populations, and are in
fact known only for a few taxa outside of mice, includ-
ing humans (Homo sapiens,Wedekind et al. 1995; Ober
et al. 1997), Atlantic salmon (Salmo salar,Landry et al.
2001), and three-spined sticklebacks (Gasterosteus aculea-
tus,Reusch et al. 2001). The behavior of wild animals (es-
pecially mammals) tested in a laboratory context is often
difficult to interpret biologically (Manning, Potts, Wake-
land, and Dewsbury 1992). It is extremely fortunate that
MHC mating preferences were initially discovered at all in
inbred strains of mice, since choosy behavior contradicts
years of artificial selection to create individuals that mate in-
discriminately with their cage mate. Seminatural population
experiments have proved successful for studying MHC-
based behavioral phenomena in two of the four species for
which MHC-based mating preferences are known: house
mice (Potts et al. 1991) and Atlantic salmon (Landry et al.
2001). As animal biologists begin to appreciate the value of
this ecological compromise between the laboratory and the
field, we expect there will soon be many creative designs for
adapting this powerful technique to study other biological
traits in a population context.Case 2: Fitness Consequences of Inbreeding in MusThe primary cause of inbreeding depression is the expres-
sion of deleterious recessive alleles (Roff 2002), which are
expressed at a higher rate in inbred individuals (Latter
1998). The deleterious effects of inbreeding have been ap-
preciated for centuries. As schoolchildren we usually learn
about it through the example of the intermarriage of royal
lineages in Europe and the consequent increased incidence
of genetic diseases (e.g., hemophilia) in these inbred line-
ages (Shaw 2001). The near universal presence of incest ta-
boos in human societies and the myriad ways in which
plants and animals avoid inbreeding (Pusey and Wolf 1996)
suggest that inbreeding has been an important and persis-
tent problem to most life forms. However, the actual fitness
consequences in nature have been poorly characterized, and
some authors have even suggested that inbreeding has no to
little effect on animal fitness in the wild (Shields 1982). Sim-
ilarly, the consequences of inbreeding in humans at the level
of cousin unions have been deemed so minor that guidelines
for discouraging such unions have recently been relaxed
(Bennett et al. 2002). Consistent with this view are the
apparent successes of naked mole-rats, a striking example
of a highly inbred rodent species (Reeve et al. 1990), and
black-tailed prairie dogs, which are reported to suffer no
detectable fitness declines from inbreeding at the level of
cousins and lower (Hoogland 1992). However, in neither of
these organisms were fitnesses compared between outbred
and inbred adults engaged in direct competition. As we sub-
sequently review, by far the largest component of inbreed-
ing-associated fitness declines occurs during adulthood. In
summary, inbreeding depression is often observed, but the
actual fitness costs associated with it are uncertain.
One of the possible functions of MHC-based mating
preferences in house mice (described in Case 1) is the avoid-
ance of inbreeding. To evaluate the relative importance of
inbreeding avoidance on the evolution of MHC-based mat-
ing preferences, the fitness consequences of inbreeding must
be known. Two major inbreeding studies had previously
been conducted on house mice. From these data, the repro-
ductive consequences of one generation of full-sib matings
were estimated to be a 10% decline in litter size (Lynch
1977; Connor and Bellucci 1979). However, litter size was
the only fitness-related effect measured. Thus these estimates
of inbreeding in house mice only took into account the
effect of embryonic lethality from inbred matings, ignoring
all possible fitness defects present in the surviving inbred
offspring. At the time we started designing experiments to62 Chapter Five