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Proc. Natl. Acad. Sci. USA Vol. 87, pp. 2496-2500, April 1990 DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole-rat (cooperative breeding/eusoality//hypervariable minisateilite DNA) HUDSON K. REEVE*, DAVID F. WESTNEATt, WILLIAM A. NOONt, PAUL W. SHERMAN*, AND CHARLES F. AQUADROt *Section of Neurobiology and Behavior, Seeley G. Mudd Hall, and tSection of and Development, Biotechnology Building, Cornell University, Ithaca, NY 14853 Communicated by Richard D. Alexander, January 2, 1990 ABSTRACT Using the technique of DNA fingerprinting, MATERIALS AND METHODS we investigated the genetic structure within and among four wild-caught colonies (n = 50 individuals) of a eusocial mam- Samples. Naked mole-rats from four distinct colonies were mal, the naked mole-rat (Heterocephalus glaber, Rodentia: captured between 1977 and 1980 in southeast Kenya. Three Bathyergidae). We found that DNA fingerprints of colony- ofthe four colonies (A, B, and TT) were collected within 5 km mates were strikingly similar and that between colonies they of each other near Mtito Andei (30 S, 380 E); the fourth (K) were much more alike than fingerprints of non-kin in other was collected near Ithumba, approximately 40 kmn northwest free-living . Extreme genetic similarity within col- and across the Athi River. Mole-rats caught from the same onies is due to close genetic relationship (mean relatedness colony were housed together in a Plexiglas tunnel system; estimate ± SE, i = 0.81 ± 0.10), which apparently results from each colony was housed separately. Pups were born in three consanguineous . The inbreeding coefficient (F = 0.45 of our captive colonies (A, K, and TT); all of them were ± 0.18) is the highest yet recorded among wild . The conceived in intracolony . genetic structure of naked mole-rat colonies lends support to The DNA of 50 individual mole-rats was sampled: 23 kin and ecological constraints models for the evolution field-caught adults, 25 lab-born offspring from intracolony selection matings among a different subset of field-caught adults, and of cooperative breeding and . 2 offspring of a mating between an additional field-caught adult and a lab-born offspring of wild-caught parents. All the Naked mole-rats (Heterocephalus glaber) are virtually hair- individuals in our sample had died ofnatural causes; we were less and sightless mammals that live in large subterranean reluctant to sacrifice live or to risk injury or disease colonies [mean size, 74 individuals; range, 25 to >295 (1, 2)] by sampling tissues because of the likelihood ofjeopardizing in northeastern Africa. H. glaber are particularly interesting long-term behavioral studies (e.g., ref. 6). because they are eusocial: within a colony, only-one female DNA Extraction, Digestion, and Hybridization. Nuclear and her 1-3 mates reproduce, and the young from previous DNA was isolated from individual liver, muscle, or brain litters maintain and defend the colony and assist in rearing samples as described by Saghai-Maroof et al. (21). Approx- newborns as do workers in colonies of the social insects imately 6-8 jFg of DNA was digested with Hae III (a (1-6). Despite intense interest in this remarkable , four-base restriction enzyme), electrophoresed in a 1% aga- the genetic structure of naked mole-rat colonies is unknown. rose gel in 40 mM Tris acetate/1 mM EDTA (pH 8.0), blotted A knowledge of intracolony genetic relatedness, in particu- onto a nylon membrane, and hybridized to radiolabeled lar, is essential for understanding whether or not close wild-type M13 DNA or to Jeffreys's 33.15 or 33.6 probes kinship (7-10) underlies the extreme reproductive selfless- (which are cloned in M13; ref. 11) as described by Westneat ness (altruism) displayed by subordinate mole-rats. et al. (22). M13 hybridizations were carried out with both We investigated the genetic structure of naked mole-rat dATP-labeled and dCTP-labeled M13 probes. Each of the colonies by using DNA probes derived from tandem repeti- three DNA probes we used detects a distinct family of tive sequences in humans (11-16) and the M13 phage (17, 18) minisatellites. to detect repeat-sequence length variants (minisatellites). Scoring and Interpretation of Bands. For each probe, we These minisatellites typically are so polymorphic that they scored only prominent bands that were clearly distinct from can generate DNA "fingerprints" (individual-specific re- those obtained with the other probes. The M13 bands were striction fragment patterns), which have proven useful for scored first, followed by the 33.15 and 33.6 bands (the order assigning paternity and maternity in humans (11, 12) and of scoring does not affect our conclusions). A mean of 12.1, birds (15, 16, 19). We used three such probes (wild-type M13 9.9, and 7.3 bands were scored per individual for each of the phage DNA and A. J. Jeffreys's human-derived probes num- respective probes (Fig. 1); scored bands represented DNA bered 33.15 and 33.6) to generate DNA fingerprints of naked fragments ranging between 1.8 and 16 kilobases in size. DNA mole-rats from four field-caught colonies. We then inferred samples from a set of animals representing each colony (i.e., mean intracolony relatedness and degree of inbreeding by (i) controls) were run in multiple gels to facilitate comparisons directly estimating mean relatedness, using Pamilo and Cro- among fingerprints obtained from different gels. Samples zier's (20) regression technique, and (ii) comparing DNA from all four colonies were run side by side in each gel, and fingerprint similarity among field-caught colony members samples from a given colony were divided between gels; with that among littermate siblings conceived in within- these procedures ensured that a relatively high within-colony colony matings in the laboratory. similarity would not arise spuriously from between-gel dif- ferences in band migration rates. No variation was evident in The publication costs of this article were defrayed in part by page charge fingerprints of the same on the same or different gels payment. This article must therefore be hereby marked "advertisement" (regardless of the tissue from which the DNA had been in accordance with 18 U.S.C. §1734 solely to indicate this fact. isolated). 2496 Downloaded by guest on September 30, 2021 Evolution: Reeve et al. Proc. Natl. Acad. Sci. USA 87 (1990) 2497

PROBE FIG. 1. Examples of DNA finger- print patterns for naked mole-rats. M13 33.15 33 6 The bands represent DNA fragments of different size (kilobases, kb) that Size (kb) were obtained by cutting mole-rat nu- clear DNA with Hae III (a four-base - 7.8 restriction enzyme) and probing with _ *- r66 __ - _w _w wild-type M13 DNA (Left), Jeffreys's 4w, 33.15 probe (Center), and Jeffreys's 33.6 probe (Right). Fingerprints of _ 9 the same eight mole-rats are shown in the three panels; K, A, B, and IT 4 1 0 4 _39w^ refer to each animal's colony oforigin (colony B individuals were field- 40, ... s l, s.sI. caught animals; the others are off- 40a~~ spring of within-colony laboratory matings). In the M13 patterns, the 7.8- .4#$E~~~~~~l-"j and 6.6-kb fragments were identified as at a variable bi-allelic locus i .f :: ao;3; I and the 4.1- and 3.9-kb fragments 181 were identified as alleles at a variable ;t 211~~~~40 4 bi-allelic locus II by the multiple re- -1I8 J striction enzyme method of Jeffreys et al. (ref. 23; see Materials and

T TT B B A K II TiTT B B B A K TT T. TT B B B A K Methods).

In the M13 patterns, two fragments were identified as - F) for AA x Aa matings, 2p2(1 - p)2(1 - F) for AA X aa alleles at a variable bi-allelic locus I and two other fragments matings, 4p2(1 - p)2(1 - F) for Aa x Aa matings, and were identified as alleles at a variable bi-allelic locus II, using 4p(1-p)3(1 - F) forAa x aa matings. The expected value for Jeffreys et aL.'s multiple restriction enzyme method (23). In the modified regression estimate is equal to W - Z, where W both cases, the putative allelic fragments were never both = [(1 - F)(p3 - 6p2 + Sp + 4) + 4F]/[4(1- F)(2 - p) + 4F] absent, and they exhibited the same size difference regardless and Z = (1 - F)p(1 - p)[1 - (p/4)]/[1 - p(l - F)]. When of which of three restriction enzymes (Hae III, Alu I, or F = 0, the regression estimate reduces to [(p3 - 6p2 + 5p + HinfI) was used to cut the DNA. The latter finding suggests 4)/4(2 - p)] - p(l - p14), which is <0.50 for p > 0 (the that the two fragments were allelic by indicating that their amount of underestimation approaches zero as p becomes embedded tandem repeats had similar flanking sequences smaller). This analysis assumes single paternity; if it is (23). Sequence similarity, hence allelism, of the two putative assumed that two or three breeding males share paternity locus II bands was further suggested by the observation that equally, the expected regression estimates for F = 0 are also these two bands, unlike all the others, appeared only after always less than the true values of r = 0.375 and r = 0.333, hybridization to dATP-labeled M13 probe (all the other bands respectively, and again the amount of underestimation de- in the M13 fingerprints appeared after hybridization to both creases as the frequency decreases. dATP- and dCTP-labeled M13 probes). The modified regression method, in which heterozygotes Statistical Analyses of Mean Intracolony Relatedness and and homozygotes are indistinguishable and combined, thus Inbreeding. Relatedness estimates from loci I and II were yields conservative estimates of sibling relatedness in the obtained by using Pamilo and Crozier's method (20) of absence of inbreeding. We plotted the expected values ofthe regressing the mean allele frequency within colonies on the modified regression estimates for various values of F and allele frequency ofindividual colony members (0, 0.5, or 1.0). found that they were always less than the unmodified regres- This method extracts relatedness from that portion of the sion values when the band frequency was <0.50. To ensure genetic similarity within colonies that is not attributable to conservative estimates under inbreeding, we included in our the genetic similarity between colonies. Thus the technique analyses only variable bands that had a mean frequency of yields positive estimates only if the genetic similarity within <0.50 across colonies. colonies exceeds that between colonies. Colonies were Bands unique to individual mole-rats were excluded from weighted by their number of members, and regression mea- our analyses, because two lines of evidence indicated that sures were corrected for finite group size (20). these unique bands represented new and not For analyses ofvariable bands with unidentified alleles, we immigration of unrelated individuals into our study colonies regressed the relative frequency of colony members exhib- prior to their capture: (i) the mean proportion ofunique bands iting a given band on the individual's frequency of the band among field-caught animals (an estimate ofthe per-generation (O or 1). The expected regression estimate for full-sibling rate) was 0.013, which is close to the per-generation relatedness from a locus with inbreeding coefficient F and minisatellite mutation rates estimated for other gene frequency p for the allele (band) ofinterest, when allelic (0.004-0.010; refs. 1, 16, and 23); (ii) this proportion does not bands are unknown, was obtained according to Pamilo and significantly differ from that observed for lab-born littermates Crozier's procedure (i.e., table II of ref. 20), with three (0.005) (P > 0.23; Mann-Whitney test), among which there modifications: (i) a diploid, not haplodiploid, was was obviously no immigration. assumed; (ii) variable Y, which Pamilo and Crozier used to Twenty relatedness estimates were obtained from the represent the average allele frequency for a colony, became patterns generated by the 33.15 probe. These estimates were the average band frequency for a colony, with homozygotes based upon a minimum of four distinct loci [i.e., the maxi- and heterozygotes for the band being indistinguishable; and mum number of variable bands present together in an indi- (iii) mating frequencies were modified to include inbreeding. vidual (n = 8), divided by 2]. We extracted 4 relatedness IfA represents the allele corresponding to a given band and estimates from the original 20 estimates by ranking the latter a represents any alternative allele at the same locus, the from lowest to highest and taking the means of the 1st to 5th, mating frequencies are Fp + (1 - F)p4 forAA x AA matings, 6th to 10th, 11th to 15th, and 16th to 20th original estimates, F(1 - p) + (1 - F)(1 - p)4 for aa x aa matings, 4p3(1 - p)(1 respectively. Our ranking and averaging procedure mini- Downloaded by guest on September 30, 2021 2498 Evolution: Reeve et al. Proc. Natl. Acad. Sci. USA 87 (1990)

mizes the correlation among estimates due to allelism or present in a colony-mate was 0.99, 0.88, and 0.94 for the M13, linkage disequilibria, because estimates from alleles or loci in 33.15, and 33.6 patterns, respectively. These values are are especially likely to be similar and markedly higher than those for presumably unrelated indi- thus collapsed together into a single estimate. Furthermore, viduals of other species (Fig. 2). In fact, these values are significant linkage disequilibria appear unlikely, because considerably higher than those for siblings in humans or minisatellite loci typically are dispersed throughout the ge- house sparrows (0.4-0.6; refs. 12, 15, and 16) and approach nome [e.g., in humans (11, 24) and mice (23)]. We similarly those between highly inbred mice (23) and between monozy- extracted 2 maximally independent relatedness estimates gotic twins in cows and humans (17). from the four variable bands in the 33.6 fingerprints. The What accounts for the extremely low variation in DNA hypothesis that the mean intracolony relatedness is >0.50 fingerprints among naked mole-rat colony-mates? Colonies was tested with a Wilcoxon one-sample test by pooling the are apparently family groups, composed primarily of the distinct relatedness estimates (8 total) and determining offspring of one female (1-3). This alone would reduce whether the resultant distribution had a mean significantly fingerprint variability, because colony-mates are usually different from 0.50. close genetic relatives (e.g., sibs). However, in the absence of inbreeding, the maximal relatedness among colony mem- bers would be 0.50 (at autosomal loci). The high proportions RESULTS of variable bands that were shared among all individuals Intracolony Comparisons of DNA Fingerprints. The mean within colonies and alternatively fixed across colonies- probability that any given band in one mole-rat was also 100% for M13, 50% for 33.15, and 75% for 33.6 patterns, respectively (field-caught animals only)-suggests that the M13 Probe average relatedness among colony-mates exceeds 0.50. To test this, we estimated mean intracolony relatedness by Humans using Pamilo and Crozier's (20) regression technique. This analysis was performed on the two variable loci that we Cows identified in the M13 patterns by the multiple restriction Dogs 77777771 enzyme method of Jeffreys et al. (ref. 23; Materials and Methods). Both regressions yielded estimates of relatedness of 1.00 (Table 1). Additional relatedness estimates were Pigs obtained from variable bands with unidentified alleles by Naked mole-rats: between colonies using a (conservative) modification ofthe Pamilo and Crozier was within colonies technique (see Materials and Methods). This analysis I 1 done on four bands in the 33.6 patterns (relatedness esti- 0.0 0.2 0.4 0.6 0.8 1.0 mates, 0.58 and 1.00) and on 20 bands in the 33.15 patterns (0.28, 0.65, 1.00, 1.00). The mean relatedness estimate was 0.81 (SE for this sample was 0.10), which is significantly >0.50 (P < 0.04; Wilcoxon one-sample test). Jeffreys's Probes (33.15 & 33.6) It should be noted that we estimated mean within-colony relatedness, based on data obtained from all our field-caught Pied flycatchers animals. Estimates of relatedness between particular pairs of House sparrows colony-mates were not attempted because, as pointed out by Rooks Lynch (26), dyadic comparisons of DNA fingerprints may European bee-eaters yield unreliable estimates of kinship if there is even a mod- Corn buntings erate amount of genetic similarity among unrelated individ- Humans examined a mice p uals. It should also be noted that Lynch (26) Cows relatedness estimation procedure that was based on the Dogs overall DNA fingerprint similarity between particular pairs of Cats ,%".IXXXX animals; in contrast, our estimates of within-colony related- Pigs ,77777777-77, Horses -.1 x x 1\ 1\ 1\11l'\'\ll%.llllll'\%'\NINl Table 1. Genotype frequencies and relatedness estimates (r) for Japanese quail naked mole-rats (field-caught animals only), based on two Inbred mice Naked mole-rats: putative bi-allelic loci between colonies within colonies i C Locus I (M13) Locus II (M13) 0.0 0.2 0.4 0.6 0.8 1.0 Colony n SS SL LL n SS SL LL PROBABILITY OF K 4 0 0 1.00 3 0 0 1.00 BAND IDENTITY (Sb) B 15 0 0 1.00 10 1.00 0 0 TT 3 1.00 0 0 1 0 1.00 0 FIG. 2. Probabilities of band sharing (Sb) for DNA fingerprints of A 1 1.00 0 0 0 - - presumed non-kin from local (natural, solid bars; do- (r = 1.00) (r = 1.00) mesticated, hatched bars; laboratory strains, open bars) of 15 species of mammals and birds (data from refs. 13-18 and 23) in comparison Two putative allelic fragments at each of two loci represented in to between- and within-colony values for naked mole-rats. Finger- the M13 fingerprint patterns ofnaked mole-rats (loci I and II; see Fig. prints were made using probes derived from wild-type M13 phage 1) were identified. For each locus, S and L refer to the shorter and (Upper) or Jeffreys's 33.15 or 33.6 probes (Lower). Sb values for longer alleles, respectively. Data for locus I are based on 23 field- 33.15 and 33.6 patterns were averaged as arithmetic means. Included caught mole-rats; locus II data were obtained for only 14 field-caught for comparison are mean Sb values for mice (Mus musculus) from six animals due to accidental destruction of a filter and unavailability of laboratory strains that were sib-mated for ca. 60 generations (Sb additional DNA. Relatedness estimates from these loci were ob- values calculated from figure 1 of ref. 23). Values for humans (M13) tained with the regression method of Pamilo and Crozier (20). For were calculated from figure 1 of ref. 17. Sb is slightly or substantially analysis of variable bands with unidentified alleles, Pamilo and higher in naked mole-rats than in other wild species, except feral Crozier's method was slightly modified (see Materials andMethods); mice, which may also have low effective population sizes (25). see text for relatedness estimates. Downloaded by guest on September 30, 2021 Evolution: Reeve et al. Proc. Natl. Acad. Sci. USA 87 (1990) 2499 ness were based on analyses of the frequencies of specific The high genetic relatedness within colonies suggests that bands. naked mole-rats with close relatives. An independent Our relatedness estimate is not biased upward by the test ofinbreeding was conducted by comparing the empirical inclusion ofthe relatively distant colony (K) in the regression distribution of band-sharing probabilities for field-caught analyses. That is, colony K was not so different from the members ofthe same colony with that for littermates born in others that r was artificially inflated by its inclusion. Indeed, captivity. We found that the mean and variance in band- the mean probability of band sharing between members of sharing probabilities for field-caught members of the same colony K and members of other colonies (0.70) was virtually colony were virtually identical to those for lab-born litter- identical to that among members of the other colonies (0.72; mates conceived in within-colony matings (Fig. 3). This result colonies weighted equally). Our relatedness estimate is also implies a history of inbreeding. not biased by sex linkage; the mean probability that a given The inbreeding coefficient F, which is the probability that band in a male was also present in a female from the same two alleles randomly drawn from an individual are identical colony (0.93) was equivalent to that for comparisons between by descent, can be estimated from the formula: r = (1 + female colony-mates (0.95), and no individual bands were 3F)/2(1 + F), where r is the regression estimate of related- distributed according to the expectation from X or Y chro- ness among siblings (27); colony members are assumed to be mosome linkage (i.e., found predominantly in one sex or the offspring of a single mated pair, and inbreeding is assumed to other). result from brother-sister or parent-offspring mating. Our estimate of F from this formula is 0.45 (SE = 0.18). If it is 22 Between colonies (field-caught animals) assumed that three breeding males share paternity equally, F 1 can be estimated from the formula r = (1 + 5F)/3(1 + F), which yields an estimate of F equal to 0.56. These are the

4 highest inbreeding coefficients yet estimated for free-living mammals (28). Li (29) has shown that the equilibrium in-

'J. breeding coefficient for a population in which a fraction S of sib-matings and 1 - S of random matings occurs equals S/ 8 (4 - 3S). Thus the genetic structure ofH. glaberaround Mtito Andei is equivalent to that of a population in which .80% of matings are among siblings or between parents and offspring. Our results imply that most matings occur within colonies, but not necessarily that a preference exists for mating with 5 5 6 .65 .7 8 .55 .75 9 .gs the most highly related kin within a colony.

2 5 Within colonies (field-caught animals) Intercolony Comparisons of DNA Fingerprints. DNA fin- gerprints ofnaked mole-rats from different colonies were also quite similar (e.g., Fig. 1). The mean probability that a band in one individual was present in a member of another colony I was 0.89, 0.42, and 0.84 for the M13, 33.15, and 33.6 patterns, LU respectively. The latter two values are probably underesti- a mates because several small, closely spaced, invariant bands found in patterns for all three probes were counted only as LL M13 bands, although they may have represented distinct 5 probe-specific sequences. Thus the values for naked mole- rats from separate colonies are generally higher than the

a X probabilities of single band sharing between apparently un- i5 5 .55 .6 .65 7 .75 .8 .85 .9 .95 related individuals from natural populations of other verte- brate species (Fig. 2). Littermates (conceived in within-colony m at in gs ) DISCUSSION I Our DNA fingerprint analyses revealed extremely high ge- netic similarity within H. glaber colonies as well as similarity among colonies in the sampled area around Mtito Andei, Kenya. The latter result might be due to unusually low minisatellite mutation rates, strong selection in a uniform environment, or recent common ancestry among colonies. Our present data are not sufficient to rigorously distinguish among these hypotheses, but our estimates of the mean first The 5.5 6 65 7 .8 85 .9 95 mutation rate (above) argue against the explanation. hypothesis of strong selection in a uniform (subterranean) MOLE-RAT BAND SHARING PROBABILITIES environment (30) cannot be tested with our data. However, this hypothesis has been challenged as an explanation for low FIG. 3. Evidence of within-colony mating in naked mole-rats. levels of protein variability in fossorial rodents (31); more- Frequency distributions for mean fingerprint band-sharing probabil- over, it is likely that, relative to protein variants, minisatellite ities (averaged for the M13, 33.15, and 33.6 probes) between field- sequences have much smaller (ifany) phenotypic effects and caught members of different H. glaber colonies (98 pairwise com- so are expected to be under even less intense selection than parisons), between field-caught members of the same colony (112 proteins. pairwise comparisons), and between lab-born maternal siblings re- sulting from intracolony matings (56 pairwise comparisons). The The hypothesis of recent common ancestry currently latter two distributions are nearly identical (x = 0.94, SD = 0.04, for seems most plausible. Brett (1, 2) suggested that naked field-caught colony-mates; x = 0.92, SD = 0.04, for maternal siblings mole-rats form new colonies by fissioning, based on the from intracolony lab matings). The implication is that field-caught relatively large size of even the youngest colony he un- animals were themselves conceived in within-colony matings. earthed. This mechanism of colony formation, coupled with Downloaded by guest on September 30, 2021 2500 Evolution: Reeve et al. Proc. Natl. Acad. Sci. USA 87 (1990)

consanguineous mating and frequent colony (e.g., National Science Foundation postdoctoral fellowship in environ- due to predation or disease), could have resulted in the mental biology. relatively low minisatellite variability among our study col- onies. In addition, small effective resulting 1. Brett, R. A. (1986) Ph.D. Thesis (Univ. of London, London). 2. Brett, R. A., in The Biology ofthe Naked Mole-Rat, eds. Sherman, from the extreme restriction ofreproduction within H. glaber P. W., Jarvis, J. U. M. & Alexander, R. D. (Princeton Univ. Press, colonies might facilitate the fixation of mutant alleles through Princeton, NJ), in press. , thus also lowering [relatively 3. Jarvis, J. U. M. (1981) Science 212, 571-573. low effective population size may be a characteristic of many 4. Jarvis, J. U. M. & Bennett, N. C., in The Biology of the Naked small rodents (ref. 25 and Fig. 2), but generalizations about Mole-Rat, eds. Sherman, P. W., Jarvis, J. U. M. & Alexander, rodent effective population sizes based on DNA fingerprint R. D. (Princeton Univ. Press, Princeton, NJ), in press. data are premature]. 5. Jarvis, J. U. M. (1985) Natl. Geogr. Soc. Res. Rep. 20, 429-437. What are the 6. Lacey, E. A. & Sherman, P. W., in The Biology of the Naked implications of the remarkably high within- Mole-Rat, eds. Sherman, P. W., Jarvis, J. U. M. & Alexander, colony relatedness for the evolution of social complexity in R. D. (Princeton Univ. Press, Princeton, NJ), in press. H. glaber? Traditionally, either extrinsic (ecological) or 7. Hamilton, W. D. (1964) J. Theor. Biol. 7, 1-52. intrinsic (genetical) factors have been hypothesized to ac- 8. Michod, R. (1980) Genetics 96, 275-2%. count for the evolution of cooperative breeding and eusoci- 9. Wade, M. J. & Breden, F. (1981) Evolution 35, 844-858. ality (32-36). Naked mole-rat eusociality may have resulted 10. Bartz, S. W. (1979) Proc. Natl. Acad. Sci. USA 76, 5764-5768. from both kinds offactors. Ecological circumstances such as 11. Jeffreys, A. J., Wilson, V. & Thein, S. L. (1985) Nature (London) predation pressure (37, 314, 67-73. 38), the patchiness of the animals' 12. Jeffreys, A. J., Brookfield, J. F. Y. & Semeonoff, R. (1985) Nature food resources (large subterranean tubers), and the physical (London) 317, 818-819. barrier to solitary dispersal presented by the hard soils in the 13. Jeffreys, A. J. & Morton, D. B. (1987) Anim. Genet. 18, 1-16. mole-rats' and habitat (2, 4, 39, 40), all apparently have 14. Jeffreys, A. J., Wilson, V. & Thein, S. L. (1985) Nature (London) increased the payoffs for remaining in the natal colony 316, 76-79. relative to those for dispersing. Once a mole-rat stays at 15. Wetton, J. H., Carter, R. E., Parkin, D. T. & Walters, D. (1987) home, its personal reproduction is restricted, and its repro- Nature (London) 327, 147-149. ductive 16. Burke, T. & Bruford, M. W. (1987) Nature (London) 327, 149-152. efforts must be channeled into the dominant breed- 17. Vassart, G., Georges, M., Monsieur, R., Brocas, H., Lequarre, er's offspring instead of its own (37). The dominant A. S. & Christophe, D. (1987) Science 235, 683-684. is predicted to extract altruism from the helper just to the 18. Georges, M., Lequarre, A.-S., Castelli, M., Hanset, R. & Vassart, point at which it pays the helper to disperse (ref. 41; note that G. (1988) Cytogenet. Cell Genet. 47, 127-131. the presence of a small amount of genetic heterogeneity 19. Burke, T. (1989) Trends Ecol. Evol. 4, 139-144. within colonies suggests that dispersal at least sometimes 20. Pamilo, P. & Crozier, R. H. (1982) Theor. Pop. Biol. 21, 171-193. occurs and thus is an option for helpers). As the relatedness 21. Saghai-Maroof, M. A., Soliman, K. M., Jorgensen, R. A. & Allard, R. W. (1984) Proc. NatI. Acad. Sci. USA 81, 8014-8018. between the helper and the breeder's offspring increases, 22. Westneat, D. F., Noon, W. A., Reeve, H. K. & Aquadro, C. F. greater amounts of altruism can, theoretically, be extracted (1988) Nucleic Acids Res. 16, 4161. (41). Intranest mating (inbreeding), which occurs when the 23. Jeffreys, A. J., Wilson, V., Kelly, R., Taylor, B. A. & Bulfield, G. costs of dispersal outweigh the benefits of outbreeding (42), (1987) Nucleic Acids Res. 15, 2823-2836. increases the relatedness among siblings relative to a helper's 24. Jeifreys, A. J., Wilson, V., Thein, S. L., Weatherall, D. J. & relatedness to its own (hypothetical) outbred offspring (7-9, Ponder, B. A. J. (1986) Am. J. Hum. Genet. 39, 11-24. 25. Lidicker, W. Z. & Patton, J. L. (1987) in Mammalian Dispersal 43) and thus over evolutionary time may have promoted the Patterns, eds. Chepko-Sade, B. D. & Halpin, Z. T. (Univ. Chicago high levels of altruism displayed by nonbreeding mole-rats. Press, Chicago), pp. 144-161. To quantify this intuitive argument in terms of Hamilton's 26. Lynch, M. (1988) Mol. Biol. Evol. 5, 584-599. rule (7, 44), remaining in the nest and helping will be favored 27. Hamilton, W. D. (1972) Annu. Rev. Ecol. Syst. 3, 193-232. over dispersal and outbreeding, even if a helper does not 28. Rails, K., Harvey, P. H. & Lyles, A. M. (1986) in Conservation > Biology, ed. Sould, M. E. (Sinauer, Sunderland, MA), pp. 35-56. reproduce within the nest, provided r' sPib, where r' is the 29. Li, C. C. (1976) First Course in (Boxwood, potential helper's relatedness to the breeder's offspring di- Pacific Grove, CA). vided by its relatedness to its own outbred offspring, s is the 30. Nevo, E., Ben-Shlomo, R., Beiles, A., Jarvis, J. U. M. & Hickman, potential helper's probability of successful dispersal and G. C. (1987) Biochem. Syst. Ecol. 15, 489-502. outbreeding, P is the expected reproductive output of a 31. Schnell, G. D. & Selander, R. K. (1981) in Mammalian Population potential helper that has survived dispersal, and b is the Genetics, eds. Smith, M. H. & Joule, J. (Univ. Georgia Press, Athens), pp. 60-99. breeder's gain in reproduction due to helping. The same 32. Evans, H. E. (1977) BioScience 27, 613-617. extrinsic factor(s) may have both reduced s and increased r' 33. Koenig, W. D. & Pitelka, F. A. (1981) in and by disfavoring dispersal with consequent inbreeding; both Social Behavior: Recent Research and New Theory, eds. Alex- effects facilitate the evolution of helping (altruism). We ander, R. D. & Tinkle, D. W. (Chiron, New York), pp. 261-280. therefore hypothesize that eusociality in naked mole-rats is 34. Andersson, M. (1984) Annu. Rev. Ecol. Syst. 15, 165-189. maintained by two distinct effects of constraints on 35. Emlen, S. T. (1984) in Behavioural Ecology, eds. Krebs, J. R. & ecological Davies, N. B. (Sinauer, Sunderland, MA), 2nd Ed., pp. 305-339. dispersal. Such constraints (i) act as extrinsic factors by 36. Brown, J. L. (1987) Helping and Communal Breeding in Birds favoring group living and (ii) create an intrinsic factor-a (Princeton Univ. Press, Princeton, NJ). genetic bias toward altruism-by promoting within-nest mat- 37. Alexander, R. D., Noonan, K. M. & Crespi, B. J., in The Biology ing (inbreeding). of the Naked Mole-Rat, eds. Sherman, P. W., Jarvis, J. U. M. & Alexander, R. D. (Princeton Univ. Press, Princeton, NJ), in press. For helpful comments, we thank J. C. Avise, T. Burke, G. J. 38. Alexander, R. D., in The Biology of the Naked Mole-Rat, eds. T. R. L. Sherman, P. W., Jarvis, J. U. M. & Alexander, R. D. (Princeton Gamboa, G. C. Eickwort, S. Emlen, L. Honeycutt, J. Univ. Press, Princeton, NJ), in press. Hoogland, J. U. M. Jarvis, A. J. Jeffreys, D. W. Pfennig, J. Shell- 39. Jarvis, J. U. M. & Sale, J. B. (1971) J. Zool. 163, 451-479. man-Reeve, T. D. Seeley, G. Vassart, D. W. Winkler, and several 40. Lovegrove, B. G. & Wissel, C. (1988) Oecologia 74, 600-606. anonymous reviewers. J. U. M. Jarvis supplied two of the studied 41. Vehrencamp, S. L. (1983) Am. Zool. 23, 327-335. colonies (K and TT), and A. J. Jeffreys sent the 33.6 and 33.15 42. Waser, P. M., Austad, S. N. & Keane, B. (1986) Am. Nat. 128, probes. This study was funded by National Science Foundation 529-537. Grant BNS-8615842 (to P.W.S. and C.F.A.) and by a grant from the 43. Hamilton, W. D. (1975) in Biosocial Anthropology, ed. Fox, R. National Institutes of Health (to C.F.A.). H.K.R. was supported by (Wiley, New York), pp. 133-155. a training grant in integrative neurobiology and behavior from the 44. Grafen, A. (1984) in Behavioural Ecology, eds. Krebs, J. R. & National Institute of Mental Health. D.F.W. was supported by a Davies, N. B. (Sinauer, Sunderland, MA), 2nd Ed., pp. 62-84. Downloaded by guest on September 30, 2021