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SPACIAL DYNAMICS AND THE EVOLUTION OF SOCIAL
MONOGAMY IN MAMMALS
F. Stephen Dobson and Claude Baudoin
Department of Biological Sciences, Auburn University, 336 Funchess Hall,
Auburn, AL 36849, USA
E-mail: fsdobson@man.com
Laboratoire d'Ethologie Expérimentale et Comparée, Université Paris-Nord,
99 avenue Jean-Baptiste Clément, 93430 Villetaneuse, France
E-mail: baudoin@leec.univ-paris13.fr
Abstract: Social monogamy is an uncommon mating system among
mammalian species, and several hypotheses have been suggested to explain its
evolution. It is generally thought that low local population densities and wide
dispersion of female home ranges may facilitate social monogamy. We tested
this expectation with data on local density, home range area, and body mass for
65 mammalian species, 24 of which were described as socially monogamous and
41 as polygynous or promiscuous. We found that monogamous species
generally had lower local densities and smaller home ranges, though these
differences were not statistically significant and species broadly overlapped.
With statistical adjustments for body size and phylogeny, the species appeared
even more similar in local density and range area. Local density and home range
area showed a negative association, but this was mainly due to influences of
body mass and phylogeny. Thus, we found no support for the idea that low
population densities and wide dispersion of home ranges have favored the
evolution of monogamy. Given support for different hypotheses in individual
studies of different species, we suggest multiple causes of social monogamy in
mammals.
Key Words: body mass, female home range, local population density,
monogamy, mammals, phylogeny, polygyny, promiscuity
INTRODUCTION
Social monogamy has come to refer to the tendency of some species to
exhibit heterosexual pairs living in social cooperation, often with some sort of
pair bond (e.g., Mock and Fujioka 1990; van Schaik and Kappeler 2003).
Estimates of the proportion of mammals that exhibit social monogamy are about
5-15% of studied species (Kleiman 1977; Dobson 1982). Genetic monogamy, in
which a male and female have an exclusive mating relationship, appears much
rarer, given the mounting evidence of rates of multiple paternity and cuckoldry in
socially monogamous species (e.g., Keane et al. 1994; Sillero-Zubiri et al. 1996;
Girman et al. 1997; Goossens et al. 1998; Fietz et al. 2000). Yet, even without
the strictures of consistent mating and paternity patterns among couples,
conditions under which social monogamy evolves are poorly understood,
especially for mammalian species (Reichard and Boesch 2003). In part because
it is an unusual social system for mammals, social monogamy has attracted
considerable research attention (e.g., Whittenberger and Tilson 1980; van Schaik
and Dunbar 1990; Mock and Fujioka 1990; Komers and Brotherton 1997; Allainé
2000; Brotherton and Komers 2003; van Schaik and Kappeler 2003).
There are several hypotheses concerning the evolution of social
monogamy in mammals, and these are ably summarized by Brotherton and
Komers (2003). An early and perhaps simplest hypothesis was suggested in a
seminal review by Emlen and Oring (1977) that neither sex has the opportunity
or ability to monopolize multiple members of the opposite sex for mating, either
directly or through resource defense. In monogamous species, the potential for
polygyny should be limited because individuals are widely spaced over a
relatively uniform environment. This hypothesis suggests, then, that local
population density should be lower in socially monogamous species than in
polgynous or promiscuous species. This idea has not been directly tested with
information concerning mating system and population levels.
Other ideas, however, have been tested, and these hypotheses in general
have little support. The idea that biparental care is required for successful
reproduction has received much attention for explaining monogamy in some
species (e.g., Clutton-Brock 1989; Ribble 2003), but this idea was rejected as a
generalization in a phylogenetic analysis (Komers and Brotherton 1997). Two
other appropriate hypotheses involve the way that space is used: that males
maximize reproductive success by guarding a single female (which also might
suggest low local population density), or that joint defense of territory is
essential for successful reproduction. A final idea is that kin selection lowers
competition among offspring that are full siblings, and that this benefits mothers.
Both of the last two ideas have been rejected as impractical explanations for
social monogamy in mammals (Komers and Brotherton 2003). Thus, we are left
with two hypotheses that produce an expectation of lower local population
density in socially monogamous than polygnyous or promiscuous species.
Komers and Brotherton (1997) tested the idea that monogamous species
should be broadly dispersed by examining home range size in monogamous and
polygynous mammalian species, where females were dispersed into non-
overlapping ranges (viz., those that are not group-living). They found that
socially monogamous species had significantly smaller home ranges than socially
polygynous and promiscuous species. This information was difficult to interpret.
It was argued that small ranges of socially monogamous females should be more
clumped than in the polygynous species, thus facilitating association of a male
with more than one female. But the dispersion of the smaller ranges was not
tested, nor was local density examined. Lower population density should favor
monogamy, if it leads to less opportunity to monopolize multiple mates (Emlen
and Oring 1977). On the other hand, according to the logic of Komers and
Brotherton (1997) higher local density could produce greater dispersion of small
female home ranges, thus promoting social monogamy. Nonetheless, Brotherton
and Komers (2003) rejected space use as an explanation of social monogamy,
preferring a hypothesis based on mate guarding by males. Lower local
population densities should, other things being equal, facilitate mate guarding.
The purpose of our study was to examine both local population density
and female home range size in mammalian species. By re-examining home
range size and adding information about local density, we tested the conclusion
that female space use is the best predictor of social monogamy (Komers and
Brotherton 1997). To test this idea, we gathered information about local density
and augmented the data of Komers and Brotherton (1997). Two factors might
bias comparisons of home range size and local density in socially monogamous
versus polygynous or promiscuous species. The first is body size, which varies
widely among mammals (Silva and Downing 1995a), and the second is
phylogeny (Dobson 1985; Felsenstein 1985; reviewed by Garland et al. 2005).
We used regression techniques to examine and statistically remove the
influences of both of these potential biases, thus producing an examination of
the way that home range size and local density change with alternative mating
systems in mammals.
METHODS
We began with the data set of 184 species that Komers and Brotherton
(1997) examined, and augmented it with additional information from Mammalian
Species Accounts (American Society of Mammalogists). We also added in
information from Silva and Downing (1995b) on local density of mammalian
species. We augmented these data with limited information from the primary
literature. These sources produced 65 mammalian species with complete data
on body mass, local population density, and female home range area. These
species spanned the orders Artiodactyla, Carnivora, Lagomorpha, Primates,
Rodentia, and Soricomorpha.
Body mass, local population density and home range area were tested for
normality using the Shapiro-Wilk statistic. Body mass was taken into account via
individual ANCOVAs of local population density and home range area, with
monogamous and polygynous species the grouping variable and body mass
entered as the covariate. The same comparisons were made using the software
PDAP (Garland et al. 1992, 1993, 1999, 2005), with phylogeny taken into
account statistically via PDTREE and ANCOVA comparisons made with PDSINGLE.
Statistical distributions of expected F statistics, given the phylogeny used, were
estimated via 1000 simulations of random data using PDSIMUL and PDANOVA. F
statistics from ANCOVA were compared to those from the simulations to
determine statistical significance.
The phylogeny of mammalian orders was taken from Reyes et al. (2004)
and Springer et al. (2004). The Artiodactyla tree was taken from Matthee and
Robinson 1999, Matthee and Davis (2001), and Price et al. (2005); Carnivora
from Bininda-Emonds (1999); Lagomorpha from Stoner et al. (2003); Primates
from Purvis (1995) and Masters et al. (2006); Rodentia from Debry (2003),
Jaarola et al. (2004), Jansa and Weksler (2004), and Steppan et al. (2004); and
Soricomorpha from Symonds (2005).
RESULTS
For the 65 species with complete data for all three quantitative variables,
monogamous species (n = 24) did not differ significantly from polygynous
species (n = 41) in body mass, population density, or range area (Table 1). The
rank Wilcoxon test yields the same test statistics for the raw and log-transformed
data. Non-parametric tests were used for these comparisons, because none of
three variables were normally distributed: body mass (Shapiro-Wilk test, W =
0.44, p < 0.0001), local population density (W = 0.29, P < 0.0001), and home
range area (W = 0.36, P < 0.0001). With log-transformation, however, the data
conformed much more closely to a normal distribution: body mass (Shapiro-Wilk
test, W = 0.97, p = 0.21), local population density (W = 0.98, P = 0.35), and
home range area (W = 0.97, P = 0.19). In addition, variances were much closer
to equality (log-mass, F23,40 = 1.47, P = 0.33; log-density, F23,40 = 2.67, P =
0.01; log-range, F23,40 = 1.58, P = 0.25). Since log-mass and log density had
higher means and variances for polygynous species, the differences in variance
for log-density between monogamous and polygynous species were not likely to
confound further analyses. Nonetheless, we conservatively tested under the
assumption of unequal variances. We used log-transformed data in all further
analyses.
We examined whether body mass might be biasing the above
comparisons with ANCOVAs in which each of the two remaining variables (local
density and range area) were regressed against body mass, with social mating
system as the grouping variable (Figure 1). First, we found significant influences
of body mass on both local population density and home range area (local
density, R2 = 0.476, F1,63 = 57.22, P < 0.0001; range area, R2 = 0.705, F1,63 =
150.32, P < 0.0001). Second, for both local density and range area, slopes were
not significantly different for socially monogamous and polygynous or
promiscuous species (interaction of mating system and body mass: local
density, F1,61 = 2.83, P = 0.10; range area, F1,61 = 0.74, P = 0.39). Adjusted
means of monogamous and polygynous species were also not significantly
different (main effects of mating system: local density, adjusted means = 1.19
and 1.18, F1,62 = 0.00, P = 0.99; range area, adjusted means = 0.50 and 0.79,
respectively, F1,62 = 1.84, P = 0.18).
The above analyses could be biased by the structure of the historical
relationships between the species. Without adjustment for phylogeny, local
density and body mass were significantly associated (r = -0.690, n = 65, P <
0.0001), and range area and body mass were significantly associated (Pearson’s
r = 0.835, n = 65, P < 0.0001). We used phylogenetically independent contrasts
to examine the relationship between body mass and local density, and between
body mass and range area. Even when phylogeny was taken into account via
phylogenetic regression, local density and body mass were still significantly
associated (r = -0.345, n = 64, P < 0.01), as were range area and body mass (r
= 0.598, n = 64, P < 0.0001).
We took body size into account in a phylogenetically adjusted ANCOVA of
the monogamous and polygynous species. Socially monogamous species were
not significantly different in local population density from polygynous species
(compare F1,62 = 0.00 to F1,62 = 1.14 for random data, P = 1.00), nor were they
significantly different in home range size (compare F1,62 = 2.16 to F1,62 = 1.32 for
random data, P = 0.39). In both cases, slopes of local density or range area
regressed on body mass of socially monogamous and polygynous species were
not significantly different (local density, compare F1,61 = 0.59 to F1,61 = 1.18 for
random data, P = 1.00; range area, compare F1,61 = 2.82 to F1,61 = 1.25 for
random data, P = 0.21).
Because Komers and Brotherton (1997) had found that socially
monogamous species had significantly smaller ranges than polygynous or
promiscuous species, we also examined the complete data set for this difference.
In unadjusted data, body mass and range area were not significantly different
for socially monogamous and polygynous species (mass, means = 5.9 and 16.7
kg, n= 50 and 79, respectively, Wilcoxon statistic 3481.5, P = 0.12; range area,
means 1037.4 and 1116.0 ha, n = 50 and 79, respectively, Wilcoxon statistic
3272.5, P = 0.92). After log-transformation and taking body mass into account,
the overall regression was still highly significant (R2 = 0.623, F2,123 = 101.80, P <
0.0001), but there was no significant difference between the adjusted means for
monogamous and polygynous species (adjusted means = 0.90 and 1.10,
respectively, F1,123 = 1.38, P = 0.24). Slopes of socially monogamous and
polygynous species were not significantly different (F1,122 = 0.34, P = 0.56).
Finally, we examined the relationship between local population density
and home range area in the mammalian species for which we had complete
data. These variables were strongly and negatively correlated in unadjusted but
log-transformed data (r = -0.719, n = 65, P < 0.0001), and for socially
monogamous (r = -0.648, n = 24, P < 0.001) and polygynous or promiscuous
species (r = -0.745, n = 41, P < 0.0001). We regressed local density and range
area separately on body mass, and used the regression residuals from each
analysis as a “body mass adjusted” index of local density and range area. These
indices were also significantly correlated, but to a lower degree (r = -0.356, n =
65, P = 0.004). We examined these indices using phylogenetic independent
contrasts, and the correlation dropped even further and became non-significant
(r = -0.213, n = 64, P = 0.09).
DISCUSSION
There appeared to be substantial differences between local population
density and home range area of socially monogamous and polygynous
mammalian species, but these were not significant (Table 1). Both variables
were non-normally distributed and substantially influenced by body mass.
Accounting for both of these problems did not change the result of little
difference in range area and local density for monogamous and polygynous
species, but rather made it clear how little difference there really was (Figure 1).
If anything, accounting for phylogeny brought socially monogamous and
polygynous species even closer together in their range area and local density.
Under no conditions were socially monogamous and polygynous species
significantly different in local density or range area. We conclude from these
results that there are probably not great differences in use of space by socially
monogamous and polygynous species of mammals, at least given present data.
Rejection of the idea that monogamous species occur sparsely on the
ground casts doubt on the idea of Emlen and Oring (1977) that environmental
potential for polygyny is lower in monogamous species. In fact, several socially
monogamous species are genetically promiscuous (e.g., review by Allainé 2000).
Thus, there is little evidence from either local population density or home range
size that males of socially monogamous species cannot contact more than one
female during the breeding season. Other explanations must thus be sought to
explain social monogamy, at least for some species. A key might come from the
fact that although such species initially appeared to be genetically monogamous
from behavioral observations outside of the day of estrus of females, various
levels of promiscuous genetic contribution occur. Thus, mating opportunities
must be more abundant than the apparent social monogamy implies.
Remember that for the above comparisons, only species where females
are dispersed in home range (i.e., largely non-overlapping females) were
considered. There are a few species, however, in which females overlap spatially
and live under social monogamy: e.g., Alpine marmots (
Marmota marmota
,
Allainé 2000), acuchis (
Myoprocta exilis
, Dubost 1988), dwarf mongooses
(
Helogale parvula
, Creel and Waser 1991), wolves (
Canis lupus
, Sillero-Zubiri et
al. 1996; Jedrzejewski et al. 2007), and African wild dogs (
Lycaon pictus
, Frame
et al. 1979). In these species, it appears that there is reproductive suppression
if females are forced to produce young together, something that may also occur
in polygynous species, though perhaps to a lesser degree (e.g., Armitage 1998).
Nonetheless, when females commonly live in overlap, the common mating
system is polygyny or promiscuity (Komers and Brotherton 1997). Reproductive
suppression may reflect competition among females that must occur for group-
living species to exhibit social monogamy, otherwise they would be polygynous.
Our results supported Brotherton and Komers (2003) rejection of spatial
dispersion as an explanation of monogamy. Contrary to the suggestion of
Komers and Brotherton (1997), there was little evidence to suggest that female
space use is the best predictor of monogamy. If lower home range size of
socially monogamous species were associated with greater population density,
then greater dispersion of females might occur, thus supporting the spatial
dispersion prediction. While there was generally a tradeoff of home range size
and local population density among both monogamous and polygynous species,
this turned out to be due primarily to differences in body size among the species
and to phylogeny.
The explanation that Brotherton and Komers (2003) preferred was that of
mate guarding as the primary factor leading to mammalian monogamy, and our
finding that spatial dynamics exhibit great variation but no consistent pattern
with respect to local density and range area do not support their hypothesis.
Unfortunately, mate guarding occurs in polygynous species as well as
monogamous species (e.g., Kummer 1968). One might think that species with
mate guarding that occur at lower densities might by default end up as socially
monogamous. Though this might occur in some cases, there is no general
evidence for the requirement of relatively lower density or greater dispersion of
home range that would facilitate mate guarding of single females in those
species that are socially monogamous.
Mating system concepts have been fitted into an old concept of
monogamy and polygyny (e.g., Emlen and Oring 1977; Wittenberger and Tilson
1980). In some ways this is unfortunate, because it may bias our view of the
essential elements of mating interactions, and the behaviors and environments
that surround them. It might be more accurate and informative to consider the
roles of the sexes separately. Males may be examined along a scale of pair
bonding, from strongly bonded males to un-bonded males. Strongly bonded
males might have single mates or multiple mates, as occur in different human
cultures. Un-bonded males are those without attachments outside of mating
interactions with females, in species such as tree squirrels or North American
pikas (e.g., Koprowski 1988; Smith and Ivins 1986). Intermediate species would
have shorter and weaker bonds, such as males that attend females just before
their estrus periods, but not at other times (e.g.,
Spermophilus columbianus
,
Manno et al. 2007; F.S. Dobson and A. Nesterova, unpublished observations).
Species along this axis might be constrained by their genetic and neurobiological
inheritance, or might show phenotypic flexibility according to environmental
circumstances.
Females could also be placed along a scale, from those that usually mate
singly to multiple mating females. Females that mate singly could be associated
with paternal investment in young or with male defense (e.g., Richardson 1987;
Brotherton and Komers 2003; Ribble 2003). Such females produce either
monogamy, depending on whether males are mating singly or multiply as well,
or polygyny. Females that mate multiply might be attracting benefits such as
paternal care from more than one male, or they could be improving the genetic
composition of their cohort of young, depending on the number of young that
the species usually produces. Naturally, the mating patterns of both sexes would
be constrained by the social or ecological environment, such as whether males
use resources to attract females. Thus, our suggestions are not in conflict with
ideas about mate or resource defense. Rather, the division of the sexes allows a
context for understanding influences on mating systems that produce an
incredible diversity of mating and fertilization patterns, and the patterns of
parental care that attend them.
In conclusion, none of the currently described hypotheses presents a
satisfying general explanation of social monogamy in mammalian species. This
may indicate that a new approach is needed. Although five reasonable
hypotheses have been suggested, additional hypotheses may be discovered or
imagined. Alternatively, social monogamy may represent somewhat different
phenomena which have evolved independently in different groups of mammals,
and for which a unique or nearly unique set of circumstances occurs. In
addition, multiple causes may occur, and this hypothesis has been supported for
other patterns of behavior such as dispersal from the natal area (e.g., Dobson
and Jones 1985). In either event, generality is not to be expected, and one or
more of the existing hypotheses may be supported for specific cases. For
example, paternal care in the nest appears to be fairly important to monogamy
of California mice (Ribble 2003, 2007). However, in elephant shrews and Kirk’s
dik-dik, where paternal care is absent, mate guarding may prove to be the
strongest factor favoring monogamy (Brotherton and Komers 2003; Rathbun and
Rathbun 2006). Furthermore, male defense against infanticide could lead to
social monogamy in some primates (van Schaik and Dunbar 1990). The best
generality may be that many factors are involved in the evolution of social
monogamy in mammals.
ACKNOWEDGMENTS
We thank N. Rajamani and H. Trevino for assistance with searching the
literature and with data entry. This study was funded by invited professorships
from Université Paris-Nord in 2004 and 2007.
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Table 1. Body mass, home range area, and local population density for
mammalian species that are socially monogamous or are polygynous or
promiscuous. Sample sizes are 24 socially monogamous and 41 polygynous or
promiscuous species.
MEAN
BODY
MASS
± 1SD
MEAN
LOCAL
DENSITY
± 1SD
MEAN
RANGE
AREA
± 1SD
SOCIALLY
MONOGAMOUS
2.8kg
4.0kg
117.6/ha
505.1/ha
30.6ha
87.1ha
POLYGYNOUS/
PROMISCUOUS
15.3kg
33.7kg
402.5/ha
1381.7/ha
841.5ha
2043.3ha
Wilcoxon test
Statistic
Probability
733.0
0.43
823.0
0.68
700.5
0.22
Figure 1. a) Local population density regressed against body mass. b) Home
ranges area regressed against body mass. Circles are socially monogamous
species and diamonds are polygynous or promiscuous species. Linear regression
lines are fit: the shorter lines are the monogamous species. All data were log-
transformed before analyses. Statistical comparisons and adjusted means
appear in the text. For both comparisons, 24 socially monogamous and 41
polygynous or promiscuous species of mammals are represented.
a)
-2
0
2
4
-3 -2 -1 0 1 2 3
Log Mass
Log Density
-2
0
2
4
-3 -2 -1 0 1 2 3
Log Mass
Log Density
b)
-4
-2
0
2
4
-3 -2 -1 0 1 2 3
Log Mass
Log Range
-4
-2
0
2
4
-3 -2 -1 0 1 2 3
Log Mass
Log Range
