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Behavioral Ecology Vol. 11 No. 1: 7-12
© 2000 International Society for Behavioral Ecology
Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating
Biology Department, Washington University, St. Louis, MO 63130, USA, and The International Center for Tropical Ecology, University of Missouri-St. Louis, St. Louis, MO 63121, USA
Address correspondence to S. Braude, Biology Department, Washington University, One Brookings Drive, Box 1137, St. Louis, MO 63130, USA. E-mail: braude{at}biology.wustl.edu .
Received 6 March 1999; accepted 18 May 1999.
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ABSTRACT |
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Early field work on naked mole-rats, Heterocephalus glaber, suggested that small colonies are rare and that colonies can only form by fissioning of existing colonies. Many researchers expected that this would result in extreme inbreeding and high relatedness within colonies and would thus explain the evolution of eusociality in naked mole-rats. Here I report evidence of dispersers and outbreeding in colonies of wild naked mole-rats that suggests that inbreeding is not the system of mating for this species and that outbreeding is probably frequent. Wild dispersers have the same morphology as was reported for dispersers in laboratory colonies. Low levels of genetic variation in previous molecular genetic studies of naked mole-rats probably result from the viscous population structure typical of fossorial rodents.
Key words: dispersal, eusociality, Heterocephalus glaber, inbreeding, naked mole-rat.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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After Hamilton (1964
) used haplodiploidy in
the eusocial Hymenoptera to demonstrate the predictive power of inclusive
fitness, other researchers attempted to find genetic mechanisms to explain the
evolution of eusociality in other taxa (e.g.,
Lacy, 1980). Bartz
(1979) suggested that
iterations of inbreeding and outbreeding could help explain the origins of
eusociality in prototermites. Inbreeding and unusually high degrees of
relatedness have also been invoked to help explain eusociality in naked
mole-rats, Heterocephalus glaber.
The hypothesis that naked mole-rats typically inbreed developed from the
failure of early field researchers to capture small, isolated colonies,
leading to the conclusion that new colonies originate only by the fissioning
of existing colonies because pairs of naked mole-rats would not be able to
survive long enough to produce a workforce of offspring
(Brett, 1991;
Jarvis, 1985). We assumed that
even in new colonies reproductive individuals would be mating with close
relatives, such as parents or siblings. In the context of the preliminary
field reports, the low levels of genetic variation found within colonies
appeared to result from consanguineous mating. Sherman et al.
(1992: 78) concluded that
"because of inbreeding, siblings are extremely closely related, and
thus, as noted by Hamilton for eusocial Hymenoptera, a worker mole-rat reaps
genetic returns for helping them." These conclusions were based on both
a limited knowledge of the demography of wild naked mole-rat populations and
on the low levels of genetic variation reported for this species
(Faulkes et al., 1990;
Honeycutt et al., 1991;
Reeve et al., 1990). The
inbreeding hypothesis is appealing because of its genetic basis, and it has
been the focus of popular and textbook accounts of the evolution of
eusociality in naked mole-rats (Brody,
1994; Freeman and Herron,
1998; Honeycutt,
1992; Jarrow and Sherman,
1996; Sherman et al.,
1992). The far more fundamental extrinsic, ecological forces
leading to eusociality, discussed by Reeve et al.
(1990) and by Alexander et al.
(1991), have been largely
ignored or downplayed. These include predation pressure, patchiness of food,
and the general harshness of the arid environment.
As knowledge of the behavior of naked mole-rats has increased, the role of
inbreeding has become less certain. In particular, O'Riain et al.'s
(1996) discovery of a male
disperser morph in captive naked mole-rat colonies suggests that fissioning is
not the only mode of colony formation. In addition, Ciszek's finding
(companion article, this volume) that captive naked mole-rats prefer to mate
with nonrelatives contradicts the assumption that inbreeding is preferred. In
this paper I report evidence that dispersal and new colony formation by
nonrelated pairs is common and that wild dispersers have the morphology
suggested by O'Riain et al.
(1996).
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METHODS |
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Animals from 54 colonies of naked mole-rats in a 6-km2 area between the Bwatherongi and Mulika rivers in Meru National Park, Kenya, were captured, marked, and released between December 1986 and June 1998. After 1987, fieldwork was restricted to the months May through August. Entire colonies were typically captured in fewer than 5 days and with minimal disturbance using modified Hickman tube traps triggered by electronic eyes (see Braude and Ciszek, 1996
,
for detailed trapping and marking methods). Animals in a particular colony were housed together in a large metal box (1.0 x 0.5 x 0.5 m) until all members of the colony were captured. Queens and their mates were typically among the last members of a colony to be trapped, and pups as small as 3 g were captured. On the day of release, I recorded weight, length, sex, and breeding status for all animals. Animals were weighed with either a Pesola hanging scale (1986-1993) or an Ohaus digital electronic balance (1994-1998). I measured body length from snout to base of the tail for all animals captured since 1988. I calculated a weight/length ratio and used this ratio as an estimate of fatness.
Male and female genitalia are visually distinguishable for sex determination. Queens are distinctive by their swollen and perforate vagina and by protruding nipples. Breeding males are more difficult to distinguish but often have pale skin color, are very thin, and have protruding penises.
Twenty-three of the marked colonies were recaptured in more than 1 year and 9 colonies were captured in more than 5 different years, but 31 colonies were only captured once. I estimated conservative disappearance and recruitment rates using only those colonies that were captured and recaptured in sequential field seasons; there were 42 such cases.
Nascent (i.e., new) colonies were captured ad libitum. The identity of a colony cannot be known with certainty until it is captured and the marked animals are identified. However, I focused the trapping efforts in places where marked colonies had typically been captured and released. Therefore, it is likely that a large proportion of nascent colonies are never trapped and recorded.
To test whether dispersers fit the morphology described by O'Riain et al.
(1996), I compared the fatness
of dispersers with their colony mates. Dispersers were not compared to all
other mole-rats in this study because there is large variance in the fatness
of mole-rats in different colonies and in different years. I ranked the
fatness of dispersers (in the year before they dispersed) and the fatness of
other workers of similar length (± 5 mm) in the colonies from which
they dispersed. The Kolmogorov-Smirnov test was performed to determine if the
ranks of the dispersers were greater than the median ranks in their natal
colonies.
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RESULTS |
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Demographic turnover
Unlike the relatively small laboratory colonies of naked mole-rats (approximately 20-40 animals) that experience relatively little turnover of individuals (Jarvis, 1991
),
wild colonies are larger (up to 290 animals;
Figure 1) and have high rates
of both recruitment and loss. Wild colonies increased by as many as 104 pups
per year (mean ± SE = 34 ± 25, n = 42 cases in which a
colony was captured in sequential years) and lost from 12% to 91% of their
workers per year (46% ± 23%, n = 42 cases). Although it is not
possible to determine what proportion of those disappearances were due to
mortality, the fates of at least 21 animals are known because they dispersed
and either formed new colonies or, in one case, migrated into a neighboring
colony (Table 1).
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Nascent colonies
Twenty nascent colonies were captured between 1988 and 1998
(Table 1). Sixteen of these
were founded by marked animals from known colonies and four were founded by
unmarked naked mole-rats. Of the nascent colonies with marked animals, five
contained males and females from different natal colonies along with their
young; two contained breeding pairs from different natal colonies but no
offspring yet; one contained two males and a female from the same natal
colony; and eight contained only a lone mole-rat who had not yet attracted a
mate (Table 1). Most of the
nascent colonies that had already bred were captured in years with good rainy
seasons or late in the season. It is possible that the others found mates
and/or bred after the annual census ended.
These small, nascent colonies (with four or fewer adults) account for 37%
of the 54 colonies in this study (Figure
1). Despite the frequency with which they arise, most of these
nascent colonies do not appear to persist for more than one year. This is not
surprising when we consider the generally low success of dispersing rodents or
moles (Anderson, 1989;
Chepko-Sade and Halpin, 1987;
Gorman and Stone, 1990).
Although the exact fate of most colonies is unknown, one of the first dispersing animals identified in this study (#483) was found dead inside a sand boa (Eryx calubrinus) that was trapped as it tried to leave the mole-rat's burrow. Sand boas have been found occasionally near other naked mole-rat burrow entrances, but this is the only case where a marked animal was found as a prey item inside a snake.
At the other extreme, there was one successful male (#1855) who dispersed from his natal colony (D) between 1988 and 1989 and was recaptured in 1998 as the breeding male in his new colony (YY) (Table 1). He had the pale, thin, elongate morphology typical of old breeding males. The time of his dispersal is known because he came from a well-studied colony that had been recaptured in 1989, 1990, 1993, 1994, and 1998. The fact that #1855 was not recaptured for 10 years suggests that we will discover additional cases of successful dispersal as monitoring of this population continues.
The naked mole-rat disperser morph
O'Riain et al. (1996)
described the naked mole-rat disperser morph as both fat and unwilling to
engage in work. They suggest that these animals are storing energy to survive
above ground until they find another colony to enter. Although behavioral data
on wild dispersers are limited, I was able to compare their morphology with
similar-sized workers by examining the trapping records from the year before
they dispersed. The relative fatness of dispersers and similarly sized workers
was ranked in the nine colonies from which dispersers were known. The class of
wild dispersers was fatter than similar length nondispersing workers in these
colonies (Kolmogorov-Smirnov test, t = 6.791, p <.001,
n = 9 colonies). This corroborates O'Riain et al.'s
(1996) description of the
disperser morph which arises in laboratory colonies.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Nascent colonies
The capture of 21 animals who left their natal colonies and of 20 different nascent colonies over an 11-year period is sufficient to revise our earlier assumptions about the possibility of dispersal and small colony formation by naked mole-rats. However, in light of Koenig et al.'s (1996
) warning about the
likelihood of underestimating dispersal frequencies and distances, this should
not be viewed as an estimate of the frequency of dispersal. It does, however,
demonstrate that dispersal is occurring regularly as part of the normal
natural history of this species.
The naked mole-rat disperser morph
Although the results of this study confirm that the disperser morph
described by O'Riain et al.
(1996) is produced in wild as
well as in laboratory colonies, the present results differ in that dispersers
of both sexes occurred in roughly equal proportions
(Table 1), whereas only 1 of
O'Riain's 19 dispersers was a female. Dispersers in this study traveled an
average of 300 m from their natal burrows, and two animals traveled more than
2 km (Table 1). However, the
likelihood of detecting dispersers decreases with distance, and therefore mean
dispersal distances are almost always underestimated
(Barrowclough, 1978).
The difference in the sex ratio of dispersers in the laboratory and field suggests that males and females may use different environmental cues to trigger development into the disperser morph. The cues that females rely on may not have been present or strong enough in the laboratory setting. Attempts to repeat O'Riain's experiments with other captive colonies may help us discover those environmental cues.
Dispersers need the extra energy reserves in their fat for starting new
burrows, but, like other rodents, they also need the energy for traveling long
distances (Nunes and Holekamp,
1996). Like various species of moles
(Gorman and Stone, 1990),
naked mole-rat dispersers move above ground and have been captured while
moving above ground at night (Heaton,
1998).
O'Riain et al. (1996)
suggested that disperser males would attempt to join established colonies.
Although this could also contribute to gene flow, our field observations show
only one case of migration into an established colony and suggest that
dispersers are more likely to become founders of new colonies. Nascent
colonies appear to be started by one or a few animals who then attract animals
who have dispersed from other colonies. Nine females and one male were each
found alone in small, isolated burrow systems apparently waiting for mates to
join them (Table 1). A number
of these females were vaginally perforate and reproductively mature at the
time they were captured. Several were retrapped within a few days or weeks,
confirming that they were alone. However, none were found to have attracted a
mate between the first and subsequent trappings.
If females frequently start the new colonies alone, how then do they
attract males? More generally, how do mole-rats find mates from other
colonies? Other fossorial rodents use thumping or vocalization to attract
mates (Nevo and Reig, 1990),
but such behavior has never been observed in wild or captive naked mole-rats
(Lacey et al., 1991;
Pepper et al., 1991). It seems
more likely that disperser naked mole-rats find each other along old, worn,
large-animal tracks (or along roads) where they typically open holes to the
surface from which soil is expelled
(Braude, 1991). Ciszek
(personal communication) has noted that captive animals often expel debris
from their toilet chambers and suggests that lone females could advertise
their presence to passing males by kicking up feces and urine-soaked soil. It
would be easy for a passing male to notice this form of chemical communication
on a narrow animal track.
Regardless of the mechanism for finding a mate, only one of the nascent colonies with more than one animal contained exclusively marked adults from the same natal colony (colony VV, Table 1), while seven contained a mixture of marked resident and unmarked immigrant adults (Table 1). Thus, naked mole-rat dispersers are likely to be outbreeding in at least 88% of the cases where we have information about the origins of breeders. It is also possible that the female of colony VV was avoiding mating with her brothers and was waiting for a non-related male to join them, as may have happened in colonies CC and HHH (Table 1).
Genetic variation in naked mole-rat populations
When successful, these dispersers should contribute significantly to gene
flow in naked mole-rat populations. Why then have various studies found little
genetic variation in naked mole-rats? Part of the reason is that a
disproportionate number of the animals in those analyses were collected south
of the Athi River (Table 2). Jarvis (1985) points out that
the Athi River has acted as a barrier to the southward spread of H.
glaber, which only radiates out approximately 35 km from the point where
they probably crossed the river. Hence, the samples from south of the Athi
likely represent the descendants of a relatively recent founder event.
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This small population of naked mole-rats south of the Athi River has
provided most of the animals for both behavioral and molecular studies of
naked mole-rats (Table 2). All
of the molecular studies independently diagnosed the relatively recent founder
event that gave rise to this well-studied population of naked mole-rats south
of the Athi River. Specifically, all of the naked mole-rats examined by
Faulkes et al. (1990) came
from south of the Athi, and they concluded that the low variation in the genes
sampled is due to a population bottleneck. They also warned that any
quantitative interpretation of their data would be invalid without data from
complete families. Reeve et al.
(1990) also noted the lower
genetic variation south of the Athi compared to the colony they sampled north
of the Athi. They suggested that this is best explained by a population
bottleneck and recent common ancestry. Honeycutt et al.
(1991) also reported low
variation in naked mole-rats due to historic demographic factors and pointed
out that there is particularly low variation in their samples from south of
the Athi (where more than 75% of their animals were collected).
Faulkes et al. (1997)
obtained naked mole-rats from six locations north of the Athi, in addition to
five colonies south of the Athi. They found less genetic variation in the
colonies south of the Athi compared to other locations in their sample. Their
analysis of mitochondrial loci showed that the population sampled south of the
Athi must have a recent common maternal ancestor.
Low local genetic variation has also been noted north of the Athi River,
but Faulkes et al. (1997)
concluded that the low overall genetic variation found in the species is due
to isolation by distance and limited gene flow. This is exactly what we find
in other fossorial rodents (Lidicker and
Patton, 1987).
Inbreeding and relatedness
Although this study and Ciszek's (companion article, this volume) suggest
that naked mole-rats often outbreed, Reeve et al.
(1990) concluded that naked
mole-rats typically inbreed and are unusually closely related within a colony.
They examined variation within and between colonies to estimate relatedness
and inbreeding in three colonies from south of the Athi and one colony from
north of the Athi as well as laboratory-bred animals. A modification of Pamilo
and Crozier's (1982)
regression method was used to estimate intracolony relatedness, which was
found to be unusually high. However, there are two potential problems with
this analysis. First, their sample of wild animals consisted of only 23
animals distributed among four colonies. Pamilo and Crozier
(1982) warned that reliability
of their estimates decreased with fewer than 20 colonies or fewer than 10
individuals per colony. Second, Reeve et al.'s
(1990) calculations of
r values for different markers ranged from 0.28 to 1.0, and they
pooled data from different locations. However, Pamilo and Crozier
(1982: 188) pointed out that
multiple estimates should yield more similar values and warned that estimates
"when applied to subgroups not forming a panmictic unit, should be
interpreted simply as indicating the amount of allelic frequency
differentiation between subgroups, and not in terms of inbreeding or identity
by descent." Because Reeve et al.
(1990) drew their sample from
colonies as far apart as 50 km that were separated by the Athi River which
isolates the Mtito Andei population, their sampling did not form a panmictic
unit.
Confusion also exists over the term "inbreeding," which has
been used to describe an array of different biological phenomena
(Jacquard, 1975;
Templeton and Read, 1994).
Reeve et al. (1990) suggest
that the genetic structure of the Mtito Andei population is equivalent to a
population in which inbreeding has occurred in 
80% of matings. They
suggest that "inbreeding is assumed to result from brother-sister or
parent offspring mating" (2499). However, their F is an
estimate of "pedigree-inbreeding" rather than the
"system-of-mating-inbreeding" (cf.
Templeton and Read, 1994).
These two terms are measures of different biological processes. The
Fp estimated by Reeve et al.
(1990: 2499) "is the
probability that two alleles randomly drawn from an individual are identical
by descent." System-of-mating-inbreeding measures deviation from
Hardy-Weinberg equilibrium in a population due to violation of the assumption
of random mating. It is important to note that system-of-mating-inbreeding is
a population parameter, not a characteristic of individuals. Pedigree
inbreeding is a characteristic of individuals of known pedigree and can vary
among individuals in a population. Pedigree inbreeding cannot be known without
pedigree information, does not require inbreeding as the system of mating, and
has a range of 0 
Fp 1, whereas system of mating
inbreeding varies from -1 FIS 1.
These two parameters can differ greatly, especially for a population with a
recent founder event. For example, Templeton and Read
(1994) found that inbreeding
as a measure of the system of mating in captive Speke's gazelle was -0.291,
while the pedigree inbreeding for the same population was 0.1490. Even when
the system of mating is avoidance of inbreeding (FIS <
0), pedigree inbreeding may be high if the effective population size is small.
Although naked mole-rats may live in colonies of up to 300 animals, the number
of breeding individuals, and thus the effective population size, is far
smaller (Reeve et al., 1990).
Thus the pedigree inbreeding tells little about the system of mating for naked
mole-rats.
Although rarely cited, Reeve et al.
(1990) conclude that the
genetic homogeneity in their sample is best explained by recent common
ancestry due to a viscous population structure. This would result in a high
Fp but not necessarily a high FIS.
Furthermore, they point out that outbreeding must occur some of the time. This
is in complete agreement with our results from wild colonies.
Genetic homogeneity, relatedness, and kin selection
The fact remains that all four of the molecular genetic studies of naked
mole-rats found low genetic variation in local populations, most of which are
north of the Athi river (Faulkes et al.,
1990,
1997;
Honeycutt et al., 1991;
Reeve et al., 1990). Although
genetic similarity can be used to estimate relatedness within families,
genetic homogeneity and relatedness are not the same biological phenomena and
have different implications for the evolution of social behavior. Traits that
enhance the direct fitness of close relatives can spread by kin selection
precisely because these alleles are likely to be present in close relatives.
In addition, traits that reduce altruism toward relatives are less likely to
spread in groups of close relatives because they would negatively impact other
carriers of the same alleles. If genetic variation in a population is already
low because of a historic bottleneck, that alone cannot foster the spread of
traits that favor kin, nor can it slow the spread of more selfish traits. This
is precisely why we do not expect the lack of genetic variation in cheetahs to
lead to social behavior. On the other hand, we can expect the behavior of
siblings or close relatives, in even extremely heterogeneous populations, to
be influenced by kin selection. If local genetic homogeneity were due to
inbreeding, then it certainly could enhance kin selection. However, if local
genetic homogeneity is due to historic bottlenecks or population viscosity, it
cannot enhance kin selection (Queller,
1992).
Although genetic hypotheses about inbreeding and unusually high relatedness
are unnecessary for understanding eusocial behavior in naked mole-rats, I am
in no way suggesting that inclusive fitness is not central to the evolution of
eusociality in this species. In fact, the evolution of eusociality in this
species depends on the normal degree of relatedness found in any family of
parents and offspring (r =.5). Yet, Hamilton's equation relies on
both the relative costs and benefits of social behavior and on relatedness.
Although Reeve et al. (1990)
discussed both the intrinsic (genetic) and the extrinsic (ecological)
components of the equation, their discussion of inbreeding and unusually high
relatedness has received the most attention.
Tolerance of inbreeding
It is clear that inbreeding is not necessary for the evolution of
eusociality in other bathyergids such as Cryptomys damarensis and
Cryptomys hottentotus Lusaka which obligately outbreed (Bennett et
al., 1994; Burda, 1995). Yet
naked mole-rats in laboratory colonies will breed with parents or siblings.
The fact that naked mole-rats inbreed in the laboratory results from the
typical lack of alternatives. Their tolerance for inbreeding without apparent
inbreeding depression is most likely due to the low genetic variation which is
already present in these populations due to population viscosity. However,
tolerance of inbreeding is different from inbreeding as a system of
mating.
Conclusions
There are strong reasons to doubt that inbreeding is the system of mating
for naked mole-rats. These include the discovery of disperser morphs in the
laboratory and in the field, the discovery of small new colonies with breeders
from different natal colonies, and the problems with earlier population
genetic analyses that indicated inbreeding. It is much more likely that the
ecological pressures restricting colony formation and successful migration
(Lacey and Sherman, 1997;
Reeve et al., 1990) are the
factors that drove naked mole-rats to eusociality. Other relevant ecological
pressures include the economic value of remaining in an established burrow
system (Alexander et al., 1991)
and more direct interspecific competition and group defense documented by
Braude et al. (1999). The whole
range of nongenetic factors contributing to the evolution of eusociality in
naked mole-rats was recognized by Alexander in his original predictions about
eusocial vertebrates that led to the discovery of eusociality in this species
(Braude, 1997). Focus on these
factors is likely to be more illuminating than genetic homogeneity has been in
understanding the evolution of eusociality in naked mole-rats.
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ACKNOWLEDGEMENTS |
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Thanks to the Office of the President of Kenya and the Officers and Staff of the Kenya Wildlife Service for permission to conduct this research in Meru National Park. This work has been generously supported by the Singapore Zoological Gardens, the American Philosophical Society, and an Alfred Sloan Foundation Postdoctoral Fellowship. Thanks also to N. Berg, D. Ciszek, and N. Mathuku, who helped capture more than 7000 naked mole-rats in Meru National Park, to A. Weisstein for statistical consulting, to R. D. Alexander and S. B. Hrdy for discussions about the different impacts of relatedness and genetic identity on inclusive fitness, and to N. Berg, D. Ciszek, R. Crozier, J. Jarvis, E. Lacey, P. Pamilo, P. Sherman, and especially A. Templeton for comments on earlier versions of the manuscript.
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