AMER. ZOOL., 27:921-927 (1987)
Behavior-Genetic Mechanisms of Population
Regulation in Microtine Rodents'
ROBERT H. TAMARIN AND MARITA SHERIDAN
Biology Department, Boston University,
Boston, Massachusetts 02215
SYNOPSIS. We examine three behavior-genetic mechanisms of vole population regulation.
Each predicts an increase in aggressive behavior among individuals as density increases.
The polymorphic behavior hypothesis predicts heritable changes in aggressive behavior
among individuals; the sociobiological hypothesis predicts heightened aggression among
nonrelatives; and the outbreeding hypothesis predicts an increase in heterozygosity-caused
aggressiveness. In order to test these hypotheses, it is necessary to know relatedness,
aggressive behavior levels, and genotypes of individuals, as well as demographic and
reproductive parameters. Aggressive levels can be obtained during paired encounters;
genotypes can be ascertained by electrophoresis; and relatedness can be determined using
radionuclides or radiotelemetry, and electrophoresis. In this paper we discuss the hypotheses, data-gathering protocols, and the ways in which the data can be used to test the
hypotheses.
INTRODUCTION
Voles, field mice, and lemmings have
been the focus of intense research for more
than a quarter of a century because of their
interesting population dynamics (Finerty,
1980). They have proven to be a focal
group in the area of population regulation
and have been of interest to applied biologists because they can do enormous agricultural damage (Byers, 1985).
Even though we still do not know what
causes vole cycles, if in fact a single cause
exists, recent interest has turned to the
importance of social interactions in regulating density. We suggest the paradigm
that all animal populations are regulated
ultimately by a limiting resource(s), such as
food, and proximally by their social behavior and organization. In addition to sociobiological theory, there is strong empirical
evidence for the role of social behavior in
inhibiting reproduction and limiting population density of breeding individuals.
This evidence comes from studies of confined rodent populations and mammals
easily observed in nature, including sciurid
rodents, ungulates, social carnivores, and
primates (summarized in Tamarin, 1983).
Similarly, the relation of territoriality to
population density has been observed in
many bird species (Watson and Moss, 1970;
Watson, 1977; Krebs and Perrins, 1978;
Boag^a/., 1979). In voles, ample evidence
exists supporting the contention that in the
peak phase of vole population growth,
numbers are limited by spacing behavior
(summarized in Tamarin, 1983, 1985). A
logical extension of this understanding is
to look for behavioral mechanisms to also
explain the vole "crash."
BEHAVIOR-GENETIC MECHANISMS OF
POPULATION REGULATION
We will examine three different hypotheses that predict that vole cycles occur
because of changes in aggressive behavior
among individuals. Each hypothesis suggests that a different mechanism causes
these changes in aggressive behavior. These
hypotheses are (1) The Polymorphic
Behavior Hypothesis (Chitty, 1967; Krebs,
1978); (2) The Sociobiological Hypothesis
(Charnov and Finerty, 1980); and (3) The
Outbreeding Hypothesis (Smith et al.,
1
1978). Each has some support although the
From the Symposium on Behavior as a Factor in the
Population Dynamics of Rodents: New Concepts and
critical predictions of each have not been
Approaches presented at the Annual Meeting of the
American Society of Zoologists, 27-30 December adequately tested. They are not necessarily
1985, at Baltimore, Maryland.
mutually exclusive.
921
922
R. H. TAMARIN AND M. SHERIDAN
The polymorphic behavior hypothesis
This hypothesis, originally developed by
Chitty (1967) predicts that as density
increases, there will be selection for more
aggressive genotypes within a population.
The hypothesis predicts that the aggressive
profile of a population will change during
a cycle and that aggressive behavior will
have a high heritability in cycling populations (Krebs, 1978).
There is some controversy as to whether aggressive behavior changes during
changes in density in vole populations. The
data are summarized by Krebs (1985). In
some populations there is a correlation
between these two variables although in
other populations there is none. Further
comparative studies as well as a better
understanding of the important variables
to measure (see below) are needed.
Most voles breed very poorly in the laboratory and thus it has been difficult to
determine heritabilities of various traits.
Anderson (1976) examined the heritabilities of behavioral and demographic parameters in Microtus townsendii in Vancouver
and came to the conclusion that aggressive
behavior was not heritable. This conclusion is especially interesting because M.
townsendii does not undergo "normal"
cycles of density (Krebs, 1978; Taitt and
Krebs, 1985). Hence Anderson's results do
not refute the importance of heritable differences in behavior in generating cycles.
A true test of the importance of heritable
aggressive behavior in causing cycles
requires the examination of the heritability of these behaviors in populations that
cycle.
The sociobiological hypothesis
Charnov and Finerty (1980) suggest that
the relatedness of neighbors changes during a cycle, resulting in changes in aggression because animals behave quite differently towards kin than towards strangers
(Carter et al, 1980; Sherman, 1981; Barash, 1982, chapter 5; Michener, 1983). If
animals are surrounded by strangers, as
they might be at high density, they will be
more aggressive. Although theoretical
studies indicate support of this model
(Warkowska-Dratnal and Stenseth, 1985),
there are no empirical data to either support or refute this hypothesis.
The outbreeding hypothesis
This hypothesis predicts that as density
increases in a vole population, animals will
move about more, leading to greater outbreeding and hence greater heterozygosity
(Smith et al, 1978). The hypothesis further
predicts that increased heterozygosity
results in increased aggressive behavior.
Initial evidence supporting this hypothesis
comes from Peromyscus (Garten, 1974). In
voles, Bowen (1982) found a decrease in
average heterozygosity among four loci
during a decline in Microtus californicus.
Gaines (1981) found no relationship
between heterozygosity and phase of the
vole cycle among five loci in M. ochrogaster.
TESTING BEHAVIOR-GENETIC
MECHANISMS OF POPULATION
REGULATION
In order to test the polymorphic behavior, sociobiological, and outbreeding
hypotheses in voles, the following data are
desirable if not essential: relatedness of all
individuals, aggressive behavior profile of
a large sample of individuals, genotypes of
all individuals for whom behavioral data
are gathered, and a background of demography and reproductive performance. We
are thus faced with gathering behavioral,
kinship, and genetic data on secretive
organisms. Steps have been taken in all
these areas.
Behavioral data
To assess whether or not there is a heritable component to dominance behavior
and to what degree changes in agonistic
encounters between individuals take place
through ecological time, paired encounters in a neutral arena can be carried out.
Social behaviors have been analyzed in the
BEHAVIOR-GENETIC POPULATION REGULATION
923
meadow vole, Microtus pennsylvanicus, by TABLE 1. Eighteen behavioral measurements made on
several investigators (Krebs, 1970; Myers voles during paired encounters in a tubular arena*
Behavior
Description
and Krebs, 1971; Colvin, 1973; Turner and
Iverson, 1973; Caplis, 1977; McElman and Latency to
Time from start of encounter to
approach
the time mice are within 5-8
Morris, 1977). We use a tubular arena
cm of each other
(Sheridan, 1987) to study the meadow vole; Approach
Movement of one animal to within
our arena is a modified version of one used
5-8 cm of the other
Nose to nose contact
by Dienske (1979) to study interspecific Naso-nasal
Naso-anal
Nose to anal region contact
competition between the field vole (M. Vocalization
Animal makes sounds
agrestis) and the common vole (M. arvalis). Upright
Long axis of the animal perpenThe tubular shape was chosen because it
dicular to substrate
Animal pounces from an upright
more closely resembles the linear charac- Pounce
position
teristics of the vole's natural runway sys- Box
Paddle of forepaws in upright potem.
sition
Tumbling and biting
Wrestle
During paired encounters, 18 different Teeth chatRapid jaw movements
behaviors are monitored (Table 1). These
ter
One animal turns at a right angle
behaviors reflect latency to engage in Side-away
to the other
exploration and interaction, and contact- Submit
Animal lies motionless on back
promoting and contact-avoiding actions Lean
One mouse lies against the side of
the other
(Sheridan, 1987). The arena is cleaned
One animal grooms the other
Groom-other
between each bout to eliminate any olfac- Groom-self
Animal grooms itself
tory cues, which we know are important to Contact
Animals not moving while within
1 cm of each other
the voles (Reich, 1982). To standardize
One animal moves from within 5—
testing conditions, all encounters are Avoid
8 cm of the other
between non-neighbors of similar sex, Chase
One animal follows within 5-8 cm
of the other
weight (age), and reproductive condition.
It is not possible to maintain proven dom* Behavior acts were modified by Sheridan (1987)
inant or subordinate fighters with field ani- from Dienske (1979), Krebs el al. (1977), and Turner
mals as is done with laboratory mice, Mus and Iverson (1973).
musculus (Van Zegeren, 1980). T o control
for seasonal effects, data are analyzed sep- ioral scores to determine how the individarately for breeding and nonbreeding sea- ual in question responds to a conspecific of
sons.
the same weight and sex, we will do supEven with sophisticated statistical anal- plementary experiments to determine what
yses, are these the correct variables to mea- the correlates are between the variables we
sure? Will they give us any degree of pre- measure and an animal's degree of domidiction regarding vole demography? Do the nance or subordination. Two animals of
animals exhibit behaviors under the con- known paired-encounter scores will be
fining circumstances of the artificial arena placed into an arena in which a resource
that reflect their natural state? For exam- is in short supply. We will initially use a
ple, a subordinate animal, when con- centrally-located food source or patch of
fronted by another animal, may act in a cover, or with males, a centrally-located
very aggressive manner. The implication cotton swab with olfactory cues from an
is that the animal is an aggressive, domi- estrus female. In these situations, one aninant animal when in fact it may be a sub- mal generally becomes the dominant one:
ordinate animal defending itself. We will it will gain access to the resource and will
attempt to overcome these problems in two prevent access by the other animal as in
the case of Mus musculus (DeFries and
ways.
First, since we are basically using behav- McClearn, 1970). We will then attempt to
924
R. H. TAMARIN AND M. SHERIDAN
TABLE 2.
Relatives
Offspring vs. one parent
Offspring vs. midparent
Half-sibs
Full sibs
Statistical determination of heritabilities (after Falconer, 1981).
Phenotypic covariance
VtVA
V<VA
V*VA + >AVD + V &
Parameter for estimating H*
H
H
H
H
=
=
=
=
2b
b
4t
2t -
(i/,V
\'*VD
+ 91/
'
£
\/y
-' Et}/ ' P
* Hfheritability in the narrow sense] = VA/Vp, where VA = additive genetic variance; VP = total phenotypic
variance; VD = dominance variance; V& = common environmental variance; b[regression slope] = (covariance
of offspring and parent)/(variance of parent); t[intra-family correlation coefficient] = (variance between
groups)/(total variance).
determine which of the variables that we
measured correlates with this dominance
stature. Correlations will give us confidence that we have measured important
variables and will give us insight as to which
field-measured variables are most important for further study. Huck and Banks
(1982) demonstrated that lemming (Lemmus trimucronatus) females prefer dominant males where dominance was ascertained during paired encounters. This test
can also be used as an assay for the significance of paired-encounter data.
We will also use a second approach which
will simply be to determine the heritability
of any and all variables. Once the data are
gathered and entered into the computer it
requires very little effort to determine the
heritabilities of all the variables using standard quantitative measures (Table 2). Since
we will have kinships (see below) we can
determine heritabilities using the regression of offspring on midparent as well as
regressions of offspring on sires or dams.
These methods factor out maternal or
environmental effects (Falconer, 1981). If
there are no significant heritability values
then the polymorphic behavior hypothesis
of population regulation is refuted. If there
are significant heritabilities then the data
support the polymorphic behavior hypothesis. We can then begin to determine the
nature of the variables that are ecologically
significant.
Relatedness data
Relatedness can now be determined in
the field using a radionuclide-electropho-
resis technique that we developed (Sheridan and Tamarin, 1986). The basic protocol of the radionuclide technique has
been published (Tamarin et al., 1983). Laboratory studies that verify radionuclide
transfer rates and biological half-lives have
been completed (Morimoto et al., 1985).
Pregnant or lactating females are injected
with combinations of microcurie quantities
of gamma-emitting radionuclides that have
recognizably different decay characteristics. We are currently using 13 radionuclides (11OmAg, 58Co, 60Co, 51Cr, 59Fe, 54Mn,
95
Nb, 125Sb, 46Sc, 75Se, 85Sr, 88Y, 65Zn) which
are injected in combinations of two. The
levels injected are below those that cause
any measurable damage of any kind either
by radiation effects or by element toxicity
(Tamarin et al., 1983).
To assess paternity we use six polymorphic electrophoretic systems. These include
two salivary amylases (Sheridan and Tamarin, 1985), a general protein, hemoglobin,
and two enzymes. Although many loci that
we can evaluate are not polymorphic in our
local meadow vole populations (Kohn and
Tamarin, 1978) even fewer than six polymorphic loci can establish paternity to a
fair degree of confidence (Foltz and Hoogland, 1981).
Other ways have also been developed for
assessing kinship in these organisms.
Radiotelemetry allows nests of lactating
females to be found. Nestlings can then be
marked directly. This technique has been
used on several vole species (Microtus ochrogaster, Getz, personal communication; M.
pennsylvanicus, McShea and Madison, per-
BEHAVIOR-GENETIC POPULATION REGULATION
925
activity in Swedish field voles (Microtus
agrestis) in the laboratory.
The sociobiological hypothesis predicts
that as density increases, individuals
increasingly become surrounded by nonrelatives, leading to increased social strife
and eventually a cyclic decline. Again, we
can test this hypothesis with the data gathHeterozygosity data
ered since we can determine relatedness of
Heterozygosity data are gathered as a
individuals in the field. To assess relatednatural outcome of our technique to assess
ness of neighbors, we can use Malecot's
paternity. Electrophoretic data are roucoefficient of kinship (Crow and Kimura,
tinely gathered on all animals captured.
1970, p. 96). If aggressive behavior is not
From these data, heterozygosities over a
heritable and if individuals are increasingly
cycle can be assessed as well as the relasurrounded by nonrelatives as density
tionship of heterozygosity to aggressive
increases, the sociobiological hypothesis is
behavior.
strongly supported. The last steps of testing this hypothesis would be to assess the
Data analysis
changes in an individual's aggressive
behavior
towards related and unrelated
If the above data are gathered over one
neighbors
as density changes and to do
cycle, we would be able to test the three
manipulation
experiments.
hypotheses of population regulation that
are here under scrutiny. We present the
Smith et al. (1978) predicted that as density increases, there is greater outbreeding
following protocol of analysis.
The polymorphic behavior hypothesis which leads to greater levels of aggressivepredicts that aggressive behavior will ness which causes the cyclic decline. We
exhibit a high heritability in cycling pop- can test both aspects of this hypothesis.
ulations. This prediction is unique and is First, with the data generated we can test
a critical one for the polymorphic behavior the relationship of aggressiveness and hethypothesis (Krebs, 1978). Analysis of the erozygosity in voles, which has not been
data will allow us to determine the heri- done before. Second, we can determine the
tability of any measurable trait because we relationship between levels of heterozywill have values for both parents and their gosity and phase of the vole cycle.
offspring enabling heritability to be calThese hypotheses are not mutually
culated as the regression of offspring on exclusive. It is feasible that potentially all
midparent (Roberts, 1967; Anderson, three mechanisms, or any combination of
1976; Falconer, 1981; Table 2). Of prime two, can be operating simultaneously. For
interest will be the heritabilities of the social example, Stenseth (1984) has suggested
behaviors that we have measured and the that kin selection can favor more aggresive
heritabilities of traits related to dispersal individuals under the circumstances that
tendency such as various social and repro- Charnov and Finerty (1980) describe at
ductive behaviors and home range size. high density. Stenseth (1984) is, in essence,
With two exceptions, heritabilities have not combining the sociobiological hypothesis
been measured before in voles. As men- with the polymorphic behavior hypothesis.
tioned above, Anderson (1976) measured Other interactions could also be envithe heritability of behavioral and demo- sioned. We view our protocol as one that
graphic traits in semi-enclosed groups of can determine the magnitude of each
M. townsendii. Also, Rasmuson et al. (1977) mechanism and thus the relative role of
measured the heritability of locomotor each in determining population processes.
sonal communication). Electrophoresis can
then be used to determine paternity. More
recently, recombinant DNA techniques
have been suggested to aid in kinship
determination (Kessler and Avise, 1985).
We await their more general utilization.
926
R. H. TAMARIN AND M. SHERIDAN
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ACKNOWLEDGMENTS
Press, Athens.
Garten, C , Jr. 1974. Relationships between behavThis work was supported by NSF Grant
ior, genetic heterozygosity, and population
DEB 8103483 and NIH Grant 1R01
dynamics in the oldfield mouse, Peromyscus polionotus. Master's Thesis, Univ. Georgia.
HD18620 to Tamarin. Helpful comments
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tus, female choice and mating success in the brown
Adler, Rick Ostfeld, and Fred Wasserman.
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