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Behavioral Ecology Vol. 11 No. 1: 1-6
© 2000 International Society for Behavioral Ecology
New colony formation in the "highly inbred" eusocial naked mole-rat: outbreeding is preferred
University of Michigan Museum of Zoology, Ann Arbor, MI 48109-1079, USA
Address correspondence to D. Ciszek. E-mail: ciszek{at}umich.edu .
Received 6 March 1999; accepted 18 May 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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If the adaptive significance of sexual reproduction derives from genetic recombination, then sexual organisms that severely inbreed minimize the benefits of sexuality without fully escaping its costs. Local populations of the eusocial naked mole-rat are extremely genetically uniform, and colonies have the highest inbreeding coefficient known for wild mammals. Because non-breeding workers cooperate to rear the queen's offspring, researchers have speculated that the inclusive fitness benefits of close relatedness outweigh the benefits of genetic recombination, thus leading to the adaptive avoidance of outbreeding. However, I show that in laboratory colonies in which each individual had an equal number of familiar siblings and unfamiliar distant kin (UDK) as potential mates, mating pairs were significantly more likely to consist of UDK. Some form of kin recognition must have been used in order for this pattern to result. Aggression was not mitigated by relatedness, however, as both fighting and cooperation occurred as frequently between siblings as between UDK. By studying the early stages of colony development I was able to investigate correlations between physical characteristics of workers and success in attaining breeding status. I also observed allonursing, hitherto unseen in this species, and suggest that it is less likely to occur later in colony development.
Key words: aggression, allonursing, cooperation, eusociality, Heterocephalus glaber, inbreeding, kin recognition, naked mole-rat, out-breeding.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Sexually reproducing animals have generally evolved to avoid inbreeding (e.g., Blouin and Blouin, 1988
; Charlesworth and
Charlesworth, 1987; Harvey and
Ralls, 1986; Pusey and Wolf,
1996), possibly because sexual recombination leads to benefits
such as increased variability of offspring
(Williams, 1975), increased
efficiency of removal of deleterious alleles from the gene pool
(Muller, 1964), and
maintenance of resistance to parasites
(Hamilton et al., 1990).
However, an intermediate level of inbreeding may maintain advantages such as
coadapted gene complexes and local adaptations (e.g.,
Bateson, 1983;
Shields, 1982), and some
models identify conditions under which the costs of avoiding inbreeding exceed
the benefits of outbreeding (e.g.,
Alexander, 1977;
Bengtsson, 1978;
Chesser and Ryman, 1986;
Waser et al., 1986). In a few
species mating is apparently random with respect to relatedness (e.g.,
Keane et al., 1996), but
consistent close inbreeding (mates having a relatedness greater than first
cousins) is rare in natural populations
(Ralls et al., 1986;
Thornhill, 1993).
Close inbreeding may occur when alternative mates are not available. For
example, in some insects mating takes place within isolated sibling groups
immediately upon emergence (Chapman and
Stewart, 1996; Cowan,
1979; Hamilton,
1967,
1993). If, however, females
later encounter and mate with unrelated males, sperm from these subsequent
matings may take precedence in fertilization, making the initial inbreeding
essentially without cost to the female. In termites new colonies are generally
founded by an unrelated mating pair but, following the death of one of the
founders, close inbreeding becomes the colony's only reproductive option
(Bartz, 1979). In one of two
proposed cases of predominant close inbreeding despite the availability of
alternative mates, Smith
(1979) predicted that
father-daughter mating should be common in fallow deer, based on a genetic
model (also see Bengtsson,
1978; Parker,
1979), but there has been no confirming evidence from behavioral
observations or paternity analysis
(Pemberton and Smith, 1985;
Smith, 1979). The only other
species proposed to have evolved to prefer close inbreeding is the naked
mole-rat.
Naked mole-rats (Bathyergidae: Heterocephalus glaber) occur in
semiarid eastern Africa and are fossorial, excavating large subterranean
tunnel systems while foraging for tubers. They are eusocial, living in
colonies of up to 295 individuals (averaging 75;
Brett, 1991), in which only one
female breeds with a small number of males, while the remaining colony members
of both sexes perform tasks necessary for the construction, maintenance,
provisioning, and defense of the colony. Workers are not obligately sterile
and become reproductively active when separated from their colony. Colonies
generally consist of nuclear families, so workers gain inclusive fitness
benefits (Hamilton, 1964) by
assisting in the production of offspring by the queen
(Jarvis, 1981;
Sherman et al., 1991).
High genetic similarity within wild naked mole-rat colonies has led to the
assumption that close inbreeding is prevalent (Faulkes et al.,
1990;
1997;
Honeycutt et al., 1991;
Reeve et al., 1990). Jarvis et
al. (1994: 49) suggested that
although most animals (including other eusocial species) have evolved
mechanisms for inbreeding avoidance, naked mole-rats are unique "... in
having mechanisms that apparently minimize the chance of ever
outbreeding." Similarly, Faulkes et al.
(1990) suggested that naked
mole-rats actively avoid outbreeding. Lacey and Sherman
(1997) briefly discussed the
possibility that naked mole-rat queens use close inbreeding to maximize
workers' effort by maximizing the workers' relatedness to the offspring.
Contributing to the conventional wisdom that naked mole-rats typically
inbreed is the belief that new colonies form through fissioning, which can be
accomplished simply by sealing off connecting tunnels. This assumption has
been based on Brett's (1991)
evidence suggesting one such case. However, new evidence indicates that
colonies are sometimes founded by unrelated dispersers
(O'Riain et al., 1996; Braude,
companion paper, this volume). Such dispersal seems risky for these small,
nearly blind, furless poikilothermic rodents due to dangers such as predation,
starvation, temperature extremes, and the apparently low likelihood of
encountering another opposite-sex disperser. Becoming a breeder through
inbreeding is a consistently available option because a small group (as small
as one male and one female) could seal itself off from the rest of the colony
or disperse a relatively short distance together and dig a new tunnel. If an
appreciable proportion of the population risks outbreeding despite the
relative safety and accessibility of inbreeding, the benefits of outbreeding
are likely substantial.
Here I report the results of a study of new colony formation designed to identify the roles of two factors in breeding status acquisition. First, the role of morphological variables in determining breeding potential is relevant to the underlying conflicts and confluences of interests that govern the evolution and maintenance of eusociality in this species. Although the production of future generations of successful breeders is the ultimate function of the colony, there may be conflict within the colony over which individuals become breeders and which remain workers. For example, if a worker can alter its physical characteristics so as to increase, compared to other workers, its likelihood of eventually becoming a breeder, this "selfish" behavioral strategy could conflict with the interests of the colony as a whole. Alternatively, if the traits that contribute to success in achieving breeding status are not under a worker's control, then most individuals will benefit from maximizing nepotistic effort. Some physical characteristics reflect the buildup of fat and/or muscle and are directly affected by a worker's behavior, whereas others, such as skeletal size, are less responsive to behavioral changes.
Secondly, I examined the role of relatedness in breeding status acquisition. Each animal in six experimental colonies was with an equal number of opposite-sex familiar (reared together) siblings and unfamiliar (never before encountered) distant kin (UDK). Familiarity was a correlate of relatedness, as is true in nature. Mating that is random with respect to relatedness should occur if naked mole-rats have no ability to distinguish degrees of relatedness of kin; conversely, nonrandomness in either direction would indicate some form of kin recognition. Consistent close inbreeding, which would constitute the first demonstration of such a preference, would pose the paradox of a sexually reproducing species that benefits from minimizing genetic recombination.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Study animals
The naked mole-rats used in this experiment (23 males, 24 females) were second- and third-generation descendants of two neighboring colonies trapped by R. D. Alexander, P. W. Sherman, and J. U. M. Jarvis in 1979 near Mtito Andei, Kenya. Several years before the current study, five separate captive colonies were formed by combining wild-caught animals from the two source colonies. In this experiment, UDK were from different captive colonies and had never interacted with each other before this study; siblings were either full or maternal half-siblings, raised to adulthood together. All animals were individually marked adult nonbreeders (workers), ranging in age from 6 to 35 months.
Three days before removing the animals from their natal colonies to form the experimental colonies I briefly anesthetized them, weighed them, and measured five morphological variables. Three were skeletal measures: body length (nose to anus), skull width (immediately anterior to the ear pinnae), and hind foot length. Two were soft tissue measures: neck width and abdomen width, each measured at the widest point. I also estimated relative levels of body fat using an electromagnetic scanner to measure total body conductance (EM/SCAN TOBEC Model SA-3000).
Experimental colonies
I formed each of the six colonies by combining two males and two females
from one natal colony (i.e., four siblings) with two males and two females
from a different natal colony (i.e., the two groups of four siblings were UDK
to each other). The average maximum age difference within experimental
colonies was 11 months. Each colony contained eight animals, four males and
four females, except colony 4 contained only three males because a fourth male
that fit the relatedness and age criteria was not available. The animals were
matched for size as closely as possible. The mean within-colony maximum
difference in mass of same-sex animals was 7.0 g (SD = 3.5 g; the mean mass of
the 47 animals was 31.0 g). In three colonies the heaviest male and the
heaviest female were siblings; in three they were UDK. Colonies 1 and 2 were
formed in February 1997 and 3-6 in February 1998.
All colonies were kept in a dimly lit room maintained at approximately 28°C. Each colony was housed in three 15-cm cubical Plexiglas boxes connected by two 75-cm glass tunnels. A heat source was placed at both ends of each colony, and food was placed in both end boxes daily. A variety of foods, mainly fruits and vegetables, were provided ad libitum. All maintenance and experimental protocols were approved by the University Committee on Use and Care of Animals.
Data collection
I recorded behaviors related to reproduction and aggression using 10-min
focal watches and ad libitum observation. During a focal watch I observed one
colony for exactly 10 min and recorded all reproductive and aggressive
behaviors. For colonies 1 and 2, I did 12 watches, all in the month after
colony formation. Each of colonies 3-6 received 10 watches in the month after
colony formation, plus 5 in July and 5 in October of 1998 (5 and 8 months
after these colonies were formed, respectively). I performed focal watches at
various times of day. Most data collection was ad libitum, meaning that I
divided my attention among the six colonies and recorded all reproductive or
aggressive behaviors. I observed the colonies in this way at least once daily
for a minimum of 10 min and up to several hours. I performed frequent,
extended periods of ad libitum observation on initial colony formation, and in
response to the occurrence of any of the following: mating behavior,
parturition, allonursing, and fighting. Ad libitum observation, performed
February 1997 through October 1998, totaled 199 h.
I performed focal watches and ad libitum observations while seated in the room approximately 1 m from the animals. As each colony's tunnel system was < 2 m long and composed entirely of clear glass and Plexiglas, all animals in a colony were visible simultaneously. They could not see me due to poor visual acuity, but could have detected me by scent or sound. My presence did not appear to disturb them, and I assumed that it would not bias the animals' mating behavior toward or against relatives.
Reproductive behaviors included the following: (1) mounting, in which a
male stands astride a female and angles his pelvis down such that his genitals
contact the female on or near her genitals; (2) mutual ano-genital nuzzling
(Jarvis, 1991;
Lacey et al., 1991), which may
be initiated by either a male or a female; (3) head mounting, in which the
male's posture is the same as in mounting but he presses his genitals to the
female's nose; and (4) attempted mounting, in which the female moves away from
a mounting male before his genitals touch her. I identified putative breeding
males based on these behaviors. Lack of genetic variation makes determination
of paternity by genetic analysis a practical impossibility
(Faulkes et al., 1997).
Aggressive behaviors, listed and described by Lacey et al.
(1991), were considered
"fighting" only if some degree of injury resulted because minor
aggressive behaviors, such as shoving, are not necessarily indicative of
future escalated aggression. Any two animals observed fighting each other were
termed a "fighting dyad." In a form of aggression not previously
described in naked mole-rats, two animals team up against a third individual
or another pair. The cooperating animals, which I call a "unison
pair," stand side-by-side facing their opponent and move in precise
unison as they repeatedly approach, threaten or bite, and retreat from the
opponent.
Although naked mole-rat colonies are usually peaceful, fighting sometimes
occurs (Clarke and Faulkes,
1997; Faulkes et al.,
1991; Jarvis,
1991; Lacey and Sherman,
1991). In response to aggression in colony 1 (which began 3 months
after colony formation), I developed a technique that allows individuals
involved in extended aggressive interactions the option of exiting the colony,
thereby avoiding further injury. I positioned an open platform at the end of a
tunnel for at least an hour, then switched it to the other end of the colony
for an hour (to avoid any bias due to position). Naked mole-rats are
subterranean and normally do not readily leave an enclosed tunnel system to
venture into an open space. During periods of fighting, however, in every case
one of the injured animals (never both) exited the colony given this
opportunity. After staying several minutes on the exit platform without
reentering the colony, any injured animal that exited was permanently removed
and housed separately, ending the aggressive interaction. The exit platform
was not removed until all colony members had encountered it and had the
opportunity to exit. Occasionally, uninjured animals (particularly juveniles)
walked onto the platform, but they did not hesitate to reenter the colony and
were not removed. This technique facilitates ethical intervention by
approximating the natural condition, in which animals have the ability to
leave their colony.
Statistics
The body conductance and morphological variables were strongly correlated
with weight, so to control for the effect of overall size I regressed each
variable against weight for the 47 animals combined. I then ranked the
residuals within sex within colony. For example, I ranked each female from
shortest to longest for her weight compared to the three other females she
competed with to become queen. Age and weight were also ranked within sex
within colony. After ranking, I pooled the data across colonies for analysis.
Mann-Whitney U tests were performed using Systat 5.2.1; logistic
stepwise regression was performed using SPSS 8.0. I used only nonparametric
tests because the data were ordinal.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Physical characteristics of breeders
Of the total 47 animals, 16 became breeders (7 females and 9 putative breeding males). Logistic stepwise regression indicated that, of the morphological variables, higher weight (p =.001) and a negative effect of neck width (p =.013) best predicted which animals would become breeders. At the time of colony formation, animals that eventually became breeders were heavier on average than were those that did not (Mann-Whitney U = 132.5, p =.013). In nine cases only one of two same-sex siblings became a breeder; in eight of these it was the heaviest of the two sibs (p =.019, binomial test, n = 9). However, five males and six females did not become breeders even though they were heavier than the breeder(s) of their sex in their colony, and in one colony neither the queen nor the breeding male was the largest animal of its sex. Nascent breeders tended to have relatively thinner necks than nonbreeders (Mann-Whitney U = 312, p =.093). There was no correlation between relative amount of body fat and breeding status achieved (Mann-Whitney U = 106.5, p =.882), and animals that became breeders were not significantly older than were those that did not (Mann-Whitney U = 183.5, p =.189).
Reproduction
I saw mounting only between UDK. Litters were produced in each of the six
colonies, with conception ranging from 1 to 7 months after colony formation
(mean = 3.7 months). I assumed conception occurred approximately 72 days
before parturition (Jarvis,
1991; Lacey and Sherman,
1991). No females other than those that gave birth were observed
engaging in ano-genital nuzzling or in any form of mounting. One female gave
birth but was never observed engaging in sexual behaviors.
Table 1 summarizes male sexual
behaviors. Male 165 in colony 2 and male 144 in colony 5 were not observed
mounting, but because some mating occurred while the animals were not being
observed, to be conservative I considered them putative breeders because they
frequently performed other sexual behaviors
(Table 1). There was a
significant tendency for putative breeding males to be UDK to the queen
(p =.019, binomial test, n = 9 breeding pairs). If this
analysis is restricted to only the males observed mounting, the tendency for
them to be UDK to the female is significant (p =.016, binomial test,
n = 6).
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Male 144 (colony 5) was the only putative breeding male that was a sibling of the queen; all others were UDK. In colony 5 the queen apparently preferred the UDK breeding male, 101, over her brother, 144. She moved away from male 144 in response to each of his attempted mountings but permitted male 101 to mount her twice (Table 1), and ano-genital nuzzling events between the queen and male 144 averaged only 5.5 s duration, whereas between the queen and male 101 they were more than twice as numerous and averaged 12.8 s duration.
In colony 1 all males other than male 181 were removed due to fighting before I developed the exit platform technique. The queen's first pregnancy was conceived after two of the males had been removed, but 2 months before male 164 was removed, so either 164 or 181 could have sired the litter. After male 164 was removed due to injury, the queen had three subsequent litters, which must have resulted from matings with male 181. For this colony, Table 1 includes only those reproductive behaviors observed before the removal of male 164. If 164 is included as a putative breeding male, then the outbreeding tendency is marginally significant (p =.055, binomial test, n = 10 breeding pairs), however, I regard 181 as the sole breeding male in colony 1 because he alone was successful in the aggressive contest for breeding status.
In colony 4 two sisters, females 140 and 143, both gave birth. I never saw
female 140 involved in any sexual behaviors, so she is not included in the
outbreeding statistics. However, if the male that mated with 143 (male 158)
inseminated both females, this would be an additional outbreeding pair. Female
143 gave birth first, to two pups that were not raised (typically <30% of
captive pups are raised: Jarvis,
1991; Lacey and Sherman,
1991). These pups nursed on both their mother and on 140 (their
aunt). Ten days later, female 140 gave birth to six pups, all of which were
raised. In the 10 days after their birth these pups were observed nursing for
a total of 31 min on 140 and 33 min on 143 (she was still lactating). Female
140 has not become pregnant again; female 143 has subsequently produced two
successful litters which she, as the only lactating female, nursed alone.
Aggression
No fighting occurred upon colony formation. Initial behaviors included
running back and forth in the tunnels, sniffing each other (particularly on
the head and in the ano-genital area), some shoving, and chirping
vocalizations. In every colony, within 24 h all the animals were sleeping or
reclining together in a single box ("nesting"). Throughout the
study, nesting was never divided according to kin subgroups. Fighting
eventually occurred in every colony, beginning 2-7 months after colony
formation. Whether between males or between females, fighting was as likely to
start after the conception of the colony's first litter as before. Animals
that fought each other were significantly more likely to be of the same sex
(n = 12 out of a possible 69 same-sex dyads) than of different sexes
(n = 4 out of a possible 92 opposite-sex dyads, X2 = 6.74,
p =.009). Two more female dyads (n = 7) than male dyads
(n = 5) were observed fighting (X2 = 0.343, p
=.558). As many siblings fought (n = 8 dyads) as did UDK (n
= 8 dyads).
Cooperative fighting by unison pairs was observed in three of the colonies and was performed by six different pairs of animals, a male and a female in five cases and two females in one case; this mixed-sex trend was not significant (binomial test, p =.192, n = 6 unison pairs). The opponent of a unison pair was male in four cases and female in five cases. Unison pairs were as likely to consist of UDK (n = 3 pairs) as siblings (n = 3 pairs).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Characteristics that allow dispersers to survive in the wild may differ from those leading to success in aggressive contests over breeding status. There is no nutritional stress in captivity, and animals in this experiment were not self-selected for "dispersing" from their natal colonies, but they did compete for breeding status. Successful outbreeding in the wild would require a combination of traits that allow an animal to survive dispersal, such as fat reserves, and traits that allow an animal to prevail in aggressive interactions, such as large size, quickness, and flexibility.
O'Riain et al. (1996) found
that, in addition to being heavier, captive animals regarded as dispersive
morphs were higher in body fat and in girth-to-length ratio than other
workers, but found no differences in skeletal variables. I found no difference
in percentage body fat and a trend toward thin necks (a fat storage location;
O'Riain et al., 1996) in
animals that became breeders, and again no difference in skeletal variables.
Although weight was a statistical predictor of future breeding status, every
colony contained at least one nonbreeder that was heavier than the breeder(s)
of its sex. It is possible that in such cases weight was less important in
determining breedership than was relatedness because it was generally the
heavier of two siblings that succeeded in becoming a breeder (i.e., if
relatedness is held constant, then weight is apparently the most important
factor). Because weight reflects traits under behavioral control (such as fat
reserves) as well as less malleable physical traits, the extent to which
workers can increase their future breeding chances by adjusting their
behavioral strategies is not yet clear.
The experimental animals consistently outbred (eight of nine putative breeding pairs, including all pairs observed mounting, were UDK), indicating that naked mole-rats are capable of discriminating between natal colony mates and other current colony mates. As occurs in the wild (Braude, companion paper, this volume), individuals in the newly formed captive colonies associated with UDK and with familiar close kin from which they had never been separated. By the time conception occurred, an average of 3.7 months after colony formation, there was some level of familiarity among all colony members. The animals could have used any correlate of relatedness to distinguish UDK from siblings; this study did not isolate the proximate mechanism.
Kin recognition may have been achieved through comparison of current colony
mates to self, to a memory of the natal environment, or to a memory of natal
colony mates. The traits compared could derive from shared genes (e.g., major
histocompatibility complex; Brown and
Eklund, 1994; Penn and Potts,
1998; but see Faulkes et al.,
1990) or shared environment (e.g., colony odor;
O'Riain and Jarvis, 1997);
these sources of information are not mutually exclusive. Despite using kin
discrimination in the context of mate choice, the animals displayed no
apparent nepotism in the forms of nesting aggregation, decreased aggression,
or cooperating to fight as unison pairs.
The case of two sisters breeding in a single colony led to allonursing,
which has not been previously reported in naked mole-rats. Because colonies
usually contain only one queen, a lactating female would normally be unlikely
to encounter pups that were not her own. However, allonursing is probably more
common early in colony development, when various pairs of animals may mate as
breeding status is being established, resulting in concurrent pregnancies.
Allonursing might enhance the likelihood of colony survival if it increases
the recruitment rate of initial litters. On the other hand, it is a
significant energy drain (up to 16% of body mass is lost during lactation;
Jarvis, 1991) for a female
competing to become queen. More data are needed to determine whether
allonursing is an adaptation or an incidental effect.
Aggression occurred mainly between individuals of the same sex and probably
constituted competition between potential breeders. Fighting between males is
generally very rare in naked mole-rat colonies
(Clarke and Faulkes, 1998;
Jarvis, 1991;
Lacey and Sherman, 1991), but
my results suggest that it is more common early in colony development. Soon
after a colony is formed, a stable male breeding hierarchy may be established,
such that if a breeding male is later removed, then the next male in line
advances with little further aggression. Initial fighting among potential
breeding males suggests that the selection of male breeders does not depend
solely on mate choice by queens.
The reproductive benefit of becoming a breeder may be greater for UDK than for siblings of an established breeder for two reasons: (1) siblings have a greater potential for gaining inclusive fitness benefits through working, and (2) siblings would suffer any costs associated with inbreeding, such as inbreeding depression. Therefore, siblings of a breeder may attempt to breed if the benefits of direct reproduction despite inbreeding are greater than the benefits of working, but the breeder's siblings should more readily abandon a dangerous breedership contest than should the breeder's UDK.
Braude's finding that dispersal is much more common than previously
realized (companion article, this volume), O'Riain et al.'s
(1996) detection of a
dispersive morph, and the outbreeding tendency demonstrated here indicate
that, as in other social bathyergids
(Burda, 1995;
Jacobs et al., 1998;
Jarvis et al., 1994;
Rickard and Bennett, 1997),
colony formation processes in naked mole-rats tend to lead to outbreeding
rather than to inbreeding. Although relatedness among colony members is a
prerequisite for the evolution of eusociality, my results imply that naked
mole-rats do not inbreed as a mechanism maximizing relatedness and hence
worker effort. Population viscosity may contribute to the high levels of
genetic similarity within colonies if new colonies are founded by individuals
from separate but nearby natal colonies. Limited dispersal distance may
reflect a balance between the costs of dispersal and the benefits of genetic
recombination. Evolution of the ability and tendency to identify and
preferentially mate with UDK suggests that outbreeding has historically been
an option for naked mole-rats and that it results in increased reproductive
success, even in this eusocial species with high levels of within-colony
genetic similarity.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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My thanks to R. D. Alexander, D. Marshall, W. Holmes, P. Myers, B. Low, and two anonymous reviewers for their comments on earlier drafts, S. Braude for sharing his knowledge of wild naked mole-rats, K. Welch for statistical advice, and T. Root and M. Burger for the use of TOBEC equipment. I was supported by a University of Michigan Rackham one-term fellowship while writing this paper.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Alexander RD, 1977. Natural selection and the analysis of human sociality. In: The changing scenes in natural sciences 1776-1976 (Goulden CE, ed). Philadelphia: Academy of Natural Sciences;283 -337.
Bartz SH, 1979. Evolution of eusociality in termites.Proc Natl Acad Sci USA
76:5764-5768.
Bateson P, 1983. Optimal outbreeding. In: Mate choice (Bateson P, ed). Cambridge: Cambridge University Press;257 -277.
Bengtsson BO, 1978. Avoiding inbreeding: at what cost?J Theor Biol 73:439-444.[Web of Science][Medline]
Blouin SF, Blouin M, 1988. Inbreeding avoidance behaviors. Trends Ecol Evol 3:230-233.
Brett RA, 1991. The population structure of naked mole-rat colonies. In: The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press; 97-136.
Brown JL, Eklund A, 1994. Kin recognition and the major histocompatibility complex: an integrative review. Am Nat 143:435-461.[Web of Science]
Burda H, 1995. Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents. Experientia 51:411-413.[Web of Science][Medline]
Chapman TW, Stewart SC, 1996. Extremely high levels of inbreeding in a natural population of the free-living wasp Ancistrocerus antilope (Hymenoptera: Vespidae: Eumeninae). Heredity 76:65-69.
Charlesworth D, Charlesworth B, 1987. Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237-268.[Web of Science]
Chesser RK, Ryman N, 1986. Inbreeding as a strategy in subdivided populations. Evolution 40:616-624.
Clarke FM, Faulkes CG, 1997. Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc R Soc Lond B 264:993-1000.[Medline]
Clarke FM, Faulkes CG, 1998. Hormonal and behavioral correlates of male dominance and reproductive status in captive colonies of the naked mole-rat, Heterocephalus glaber. Proc R Soc Lond B 265:1391-1399.[Medline]
Cowan DP, 1979. Sibling mating in a hunting wasp:
adaptive inbreeding? Science
205:1403-1405.
Faulkes CG, Abbott DH, Liddell CE, George LM, Jarvis JUM,1991 . Hormonal and behavioral aspects of reproductive suppression in female naked mole-rats. In: The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press;426 -445.
Faulkes CG, Abbott DH, Mellor AL, 1990. Investigation of genetic diversity in wild colonies of naked mole-rats (Heterocephalus glaber) by DNA fingerprinting. J Zool 221:87-97.
Faulkes CG, Abbott DH, O'Brien HP, Lau L, Roy MR, Wayne RK, Bruford MW, 1997. Micro- and macrogeographical genetic structure of colonies of naked mole-rats Heterocephalus glaber. Mol Ecol 6:615-628.[Medline]
Hamilton WD, 1964. The genetical evolution of social behavior I, II. J Theor Biol 7:1-52.[Web of Science][Medline]
Hamilton WD, 1967. Extraordinary sex ratios.Science
156:477-488.
Hamilton WD, 1993. Inbreeding in Egypt and in the book: a childish perspective. In: The natural history of inbreeding and outbreeding (Thornhill NW, ed). Chicago: University of Chicago Press.
Hamilton WD, Axelrod R, Tanese R, 1990. Sexual
reproduction as an adaptation to resist parasites. Proc Natl Acad Sci
USA
87:3566-3573.
Harvey PH, Ralls K, 1986. Do animals avoid incest?Nature 320:575-576.
Honeycutt RL, Nelson K, Schlitter DA, Sherman PW,1991 . Genetic variation within and among populations of the naked mole-rat: evidence from nuclear and mitochondrial genomes. In: The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press;195 -208.
Jacobs DS, Reid S, Kuiper S, 1998. Out-breeding behaviour and xenophobia in the Damaraland mole-rat, Cryptomys damarensis. S Afr J Zool 33:189-194.
Jarvis JUM, 1981. Eusociality in a mammal: cooperative
breeding in naked mole-rat colonies. Science
212:571-573.
Jarvis JUM, 1991. Reproduction of naked mole-rats. In:The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press;384 -425.
Jarvis JUM, O'Riain MJ, Bennett NC, Sherman PW, 1994. Mammalian eusociality: a family affair. Trends Ecol Evol 9:47-51.
Keane B, Creel SR, Waser PM, 1996. No evidence of
inbreeding avoidance or inbreeding depression in a social carnivore.Behav Ecol
7:480-489.
Lacey EA, Alexander RD, Braude SH, Sherman PW, Jarvis JUM,1991 . An ethogram for the naked mole-rat: non-vocal behaviors. In: The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press;209 -242.
Lacey EA, Sherman PW, 1991. Social organization of naked mole-rat colonies: evidence for divisions of labor. In: The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press;275 -336.
Lacey EA, Sherman PW, 1997. Cooperative breeding in naked mole-rats: implications for vertebrate and invertebrate sociality. In:Cooperative breeding in mammals (Solomon NG, French JA, eds). Cambridge: Cambridge University Press;267 -301.
Muller HJ, 1964. The relation of recombination to mutational advance. Mutat Res 1:2-9.[Web of Science]
O'Riain MJ, Jarvis JUM, Faulkes CG, 1996. A dispersive morph in the naked mole-rat. Nature 380:619-621.[Medline]
O'Riain MJ, Jarvis JUM, 1997. Colony member recognition and xenophobia in the naked mole-rat. Anim Behav 53:487-498.
Parker GA, 1979. Sexual selection and sexual conflict. In: Sexual selection and reproductive competition in insects (Blum MS, Blum NA, eds). New York: Academic Press;123 -166.
Pemberton JM, Smith RH, 1985. Lack of biochemical polymorphism in British fallow deer. Heredity 55:199-207.
Penn D, Potts W, 1998. MHC-disassortative mating preferences reversed by cross-fostering. Proc R Soc Lond B 265:1299-1306.[Medline]
Pusey A, Wolf M, 1996. Inbreeding avoidance in animals. Trends Ecol Evol 11:201-206.
Ralls K, Harvey PH, Lyles AM, 1986. Inbreeding in natural populations of birds and mammals. In: Conservation biology: the science of scarcity and diversity (Soule ME, ed). Sunderland, Massachusetts: Sinauer Associates; 35-56.
Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF,1990 . DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proc Nat Acad Sci USA 87:2496-2500.
Rickard CA, Bennett NC, 1997. Recrudescence of sexual activity in a reproductively quiescent colony of the Damaraland mole-rat, by the introduction of a genetically unrelated male—a case of incest avoidance in "queenless" colonies. J Zool 241:185-202.
Sherman PW, Jarvis JUM, Alexander RD, eds, 1991.The biology of the naked mole-rat . Princeton, New Jersey: Princeton University Press.
Shields WM, 1982. Philopatry, inbreeding, and the evolution of sex. New York: State University of New York Press.
Smith RH, 1979. On selection for inbreeding in polygynous animals. Heredity 43:205-211.[Web of Science]
Thornhill NW, ed, 1993. The natural history of inbreeding and outbreeding. Chicago: University of Chicago Press.
Waser PM, Austad SN, Keane B, 1986. When should animals tolerate inbreeding? Am Nat 128:529-537.
Williams GC, 1975. Sex and evolution. Princeton, New Jersey: Princeton University Press.
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