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Dispersal, inbreeding avoidance and reproductive success in white-footed mice
Anirn. Behav., 1988, 36, 456-465
Dispersal, inbreeding avoidance and reproductive success in white-footed mice J E R R Y O. W O L F F * , K A T H A R I N E
I. L U N D Y t
& R A M O N E BACCUS:~
*Biology Department, Villanova University, Villanova, PA 19085, U.S.A. t312 New Hackensack Rd., Poughkeepsie, N Y 12603, U.S.A. ~Biology Department, Berry College, Mount Berry, GA 30149, U.S.A.
Abstract. The dispersion pattern of 360 juvenile white-footed mice, Peromyscus leucopus, from 158 matings was monitored to determine whether dispersal was sufficient to prevent close inbreeding. Dispersal was male-biased with 20% of the daughters remaining in their natal home ranges. Dispersal of sons was not 'forced' by adult males, but may have been influenced by the presence of their mothers. One mother-son and five father-daughter pairs had overlapping home ranges during the breeding season, but the maximum number of matings among close relatives was three of 135 (2.2%). Dispersal of juvenile males was sufficient to keep close inbreeding at a minimum. Dispersal did not result from reproductive competition. Pregnant and post-lactating females frequently moved to new home ranges. The reproductive success of immigrants was the same as that of natal residents.
Considerable controversy exists over the proximate and ultimate causes of sex-biased dispersal (Greenwood 1980; Dobson 1982; Moore & Ali 1984; Packer 1985; Harvey & Rails 1986; Liberg & Schantz 1986). Greenwood (1980) proposed that in mammals, females compete for resources and therefore dispersal should be male-biased. Dobson (1982) argued that dispersal is related to the type of mating system and should be male-biased among polygynous and promiscuous mammals and show no bias in monogamous species. Liberg & Schantz (1986) used the reverse approach and concluded that natal philopatry should be female-biased in polygynous and promiscuous mammals. Packer (1979), Krohne et al. (1984), Wolff& Lundy (1985), Harvey & Rails (1986) and others argue that malebiased dispersal in mammals has evolved as a mechanism to prevent inbreeding with the more philopatric females. Moore & Ali (1984), on the other hand, countered that juvenile males disperse not to prevent inbreeding, but to reduce competition with resident adult males (but see Packer 1985). Harvey & Rails (1986) summarized these arguments and concluded that inbreeding avoidance was the most parsimonious explanation for male-biased dispersal among mammals. These results have been supported by a number of field studies on, among others, marmots (Marmota flaviventris; Brody & Armitage 1985), prairie dogs (Cynomys ludovicianus; Hoogland 1982) and the marsupial Antechinus (Cockburn et al. 1985). The deleterious effects of inbreeding are well-known
(Connor & Bellucci 1979; Rails et al. 1979; Ballou & Rails 1982; Haigh 1983a; Ralls et al. 1986; but see Smith 1979; Shields 1982; Chesser & Ryman 1986, for situations where inbreeding may be advantageous). Thus, sex-biased dispersal would be an adaptive mechanism to separate relatives prior to mating. Dispersal is common among small mammals and apparently serves a number of functions (see Gaines & McClenaghan 1980; Stenseth 1983; Lidicker 1985, for reviews). Dispersal that is dependent on density has been suggested in a number of studies, but Krohne et al. (1984), Nadeau et al. (1981), Adler & Tamarin (1985) and Wolff & Lundy (1985) concluded that dispersal among Peromyscus is more closely associated with mating behaviour than density per se. Wolff & Lundy (1985) found that juvenile male P. leucopus dispersed whereas juvenile females were more philopatric and inherited their maternal home range (see also Nicholson 1941). Dispersal of sons prevented mother-son and brother-sister matings, but daughters often had home ranges overlapping those of males who could have been their fathers. Wolff & Lundy concluded that mother-son and brother-sister matings were unlikely, but they could not reject the possibility of father-daughter matings, In an earlier study with P. maniculatus in nest boxes, Howard (1949) frequently found fathers and daughters together and concluded that inbreeding may be as high as 10%. Goundie & Vessey (1986) also found that home ranges of
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Wolff et al.: Dispersal in white-footed mice
457
Table I. Locus designations and allele frequencies for nine polymorphic presumptive loci from blood tissue found in Peromyseus leucopus Allele designation Isozyme Catalase (CAT) Carbonic anhydrase (CA) Adenosine deaminase (ADA) 6-Phosphogluconatedehydrogenase(6-PGD) Phosphoglucose isomerase (PGI) Naphthyl-AS-acetate esterase (NASA) Purine nucleoside phosphorylase (NP) Post-albumin (P-ALB) Transferrin(TRF)
siblings and of parents and offspring overlapped in a 2-ha woodlot population of P. leucopus and suggested the possibility of inbreeding. In this study we used the radionuclide-electrophoresis technique (Tamarin et al. 1983) to identify mothers, potential fathers and offspring of whitefooted mice, Peromyscus leucopus, and followed their dispersal and dispersion pattern during subsequent breeding seasons to measure the incidence of close inbreeding (parent-offspring or siblings). We also examined the effects of density, adult aggression, and the presence of adult males or female relatives on dispersal of juvenile males. These results were interpreted with respect to proximate and ultimate causation for sex-biased dispersal. Lastly, the reproductive success of natal residents (animals born on the study site) was compared with that of immigrants.
M A T E R I A L S AND M E T H O D S The study was conducted at the Mountain Lake Biological Station in Giles County, southwestern Virginia, U.S.A. (37°10'N, 80°30'W). The Station is at an elevation of 1200 m in the Allegheny Mountains in an oak-hickory-maple forest scattered with rhododendron, Rhododendron sp., thickets and an understory of ferns (primarily Osmunda spp.) and blueberry, Vaccinium spp. The behavioural ecology of Peromyscus in this region is well-known (Wolff et al. 1983; Wolff 1985a, b, c, 1986). Home ranges of males and females overlap, but are exclusive within each sex. The mating system ranges from promiscuity to facultative monogamy. Two breeding seasons occur each year,
F
M
0.101 0.011 0.008 0-461 0.433
0.488 0.608 0.416 0.989 0.992 0.126 0.556 0.975 0.943
0.029
S
S'
0.512 0.392 0.474 0.009 0.400 0.013 0.011 0.025 0.043
one in April-June and the other in SeptemberNovember. Spring-born animals breed in the autumn and autumn-born animals breed the following spring. Four 3-ha live-trapping grids were established in similar habitat within 500 m of the Station. Each grid consisted of 196 trap stations in an array of 14 x 14 with 12.5 m spacing. One large Sherman live-trap baited with solid shortening was placed at each station. Animals were trapped for 2 or 3 consecutive days at intervals of 2-3 weeks from August through November 1984, March through November 1985, and March through July 1986, and a final census was conducted in October 1986. Only three of the four grids (3, 8 and 9) were trapped in 1986. The study included three autumn and two spring breeding seasons. Animals were ear-tagged for permanent identification, and species, sex, age, weight, reproductive condition and trap locations were recorded. Females were recorded as pregnant if they had swollen abdomens and lactating if they had large nipples. Males were recorded as having scrotal or abdominal testes. A radionuclide technique was used to determine matrilineal relationships (Tamarin et al. 1983) and an electrophoretic paternity-exclusionanalysis was used to determine putative fathers (Foltz 1981). All pregnant or lactating females were injected with 15 ~Ci of iron (59Fe), strontium (8SSr), selenium (7SSe), zinc (6SZn), caesium (137Cs), manganese (lS4Mn), or chromium (51Cr) diluted in 0.5-ml saline solution (Wolff & Lundy 1985). The isotopes transferred to the young in utero and through the milk. Different isotope combinations were given to animals on the same grid. All juveniles were scanned on a multi-channel ion-isotope analyser
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Animal Behaviour, 36, 2
when they were first captured. Each radionuclide had unique spectral peaks so juveniles could be accurately assigned to their mothers and siblings. Approximately 1 ml of blood was collected from the orbital sinus of most animals. A paternityexclusion analysis was conducted by analysing nine polymorphic presumptive loci found in plasma and red blood cells using standard techniques for starch-gel electrophoresis (Table I). Tris citrate buffer pH 7.0 was used for CAT, CA, ADA, and 6PGD (Ayala et al. 1972), and lithium hydroxide was used for PGI, NASA, NP, P-ALB and T R F (Selander et al. 1971). Behavioural trials were conducted between adults and juveniles within the home range of the adults using the technique of Wolffet al. (1983) and Wolff(1985b). In each trial an adult (weighing 18 g or more and sexually mature) and a juvenile (weighing less than 18 g and not reproductive) were placed in a clear, open-bottom, Plexiglas cylinder 32 cm in diameter and 48 cm high. Each trial lasted 5 rain and three behaviours were recorded. (I) Aggression: an attack or offensive approach in which one animal attempts to displace the other, resulting in a retreat, submission, or counter attack. (2) Avoidance: one animal avoids and moves away from the other animal just because of its presence not because of any aggressive behaviour. (3) Non-aggressive contact: touching such as sniffing, crawling over each other, or huddling that does not elicit an aggressive response. Fifteen wooden nest boxes (Wolff& Durr 1986) were placed between 1 and 2 m in trees on each grid and checked periodically throughout the study. Sex, tag number, weight, and reproductive condition were recorded on nest box occupants. During the juvenile recruitment period of 15 May through 15 June 1986, all adult males were removed from grid 3. This was done to see whether juvenile males would remain in their natal home ranges if no adult males were present. Home ranges were estimated by drawing a minimum-area polygon around the trap stations where resident animals were caught three or 'more times over at least a 2-week period (Wolff 1985b). We could not separate dispersal from death in this study, but we have no evidence of sex differences in mortality among Peromyseus (Wolff & Lundy 1985). Consequently, dispersal will refer to all animals that disappeared from the grids, assuming that equal proportions of each sex died.
RESULTS
Population Density The population density (minimum number alive) of P. leucopus ranged from 15 to 20 animals/ha in 1984 and 1985, and reached a peak of 38 animals/ ha in June 1986. At any time, an additional 5-10 animals/ha of P. maniculatus occurred syntopically with P. leucopus (Wolff et al. 1983; Wolff 1985b). Trappability (Hilborn et al. 1976) was 94%.
Pregnancy and Weaning Rates A total of 306 pregnant or lactating females were caught on grids from August 1984 through June 1986. Of these females, 221 remained in residence longer than 4 weeks; long enough to wean a litter. These 221 females produced 243 pregnancies; however, only 151 females successfully weaned 158 litters. We identified 184 sons and 176 daughters of these 151 females. The mean number of weaned offspring per successful litter (at least one young weaned) was 2.4. Mean litter size for P. leucopus is 3.4 (Wolff 1986) so weaning rate was 70%. An additional 55 sons and 47 daughters were found in nest boxes or had isotopes indicating they were born on the grids, but they could not be accurately assigned to any mother. Of those females that successfully weaned at least one young, 27 disappeared after a 3-week lactation period, 84 stayed in their same home range after weaning, and 40 were on the edge of grids and their fate could not be determined. Fortyeight females disappeared while pregnant and 23 females immigrated while they were pregnant and were within a couple of days of parturition.
Residency, Dispersal and Inbreeding The mean length of residence was determined for 246 animals that were initially caught on the grids from April through June 1985. Animals on the edge of grids were excluded from the analysis. The mean lengths of residence were not significantly different for adult males (9-2 weeks+0-70 so, N=77) and females (9.2 weeks___0-74 so, N = 68; Mann-Whitney U-test, z=0-076, P=0-94), but they were different for juvenile males (4.4 weeks+0.49 so, N = 54), and juvenile females (7.5 weeks+ 1-00 SD, N=47; z=2.012, P=0'044). The number of juvenile males and females moving onto grids during the May-July 1985
Wolff et al.: Dispersal in white-#ooted mice
459
Table lI. The number of juvenile male and female P. leucopus that
immigrated to open grids during three breeding seasons Spring 1 9 8 5 Grid no. Males Females 3 8 9 16 Total
18 18 31 16 83
8* 7* 11" 14 40*
Autumn 1985
Spring 1986
Males Females
Males Females
26 12 15 17 70
13" 14 19 24 70
45 38 23 -106
24* 24 22 -70*
* For differences between males and females for each grid and season )C~ >3.48, df= 1, P<0.05. Table I!I. The number and (percentage) of animals present on a grid in one breeding season that remained in their same home range until the subsequent breeding season
Age/sex Fathers Mothers Present in autumn 1984 Remained until spring 1985 Present in spring 1985 Remained untilautumn 1985 Present in autumn 1985 Remained until spring 1986 Present in spring 1986 Remaineduntilautumn 1986 Total All breeding seasons Next breeding seasons
Sons
Daughters
36 14 (39) 49 10 (20) 47 9 (19) 44 2 (5)*
23 8 (35) 41 8 (20) 28 7 (25) 59 8 (14)
24 1 (4) 54 2 (4) 23 2 (9) 83 9(ll)t
21 10 (48) 47 7 (15) 38 8 (21) 70 10 (14)
176 35 (20)
151 31 (21)
184 14 (8)
176 35 (20)
* All adult males were removed from grid 3. t Six of nine sons were on grid 8.
recruitment period was 83 a n d 40, respectively (Table II). W i t h a 1 : 1 sex ratio in the p o p u l a t i o n (Wolff 1986), these values were significantly different o n three o f four grids. Sex ratios of juvenile i m m i g r a n t s were similar o n three of four grids in a u t u m n 1985, with only grid 3 showing a significant influx o f males. In spring 1986, i m m i g r a t i o n favoured males o n two of three grids, b u t was significant only on grid 3. A l t h o u g h a considerable n u m b e r of females dispersed a n d immigrated, the general trend was for greater i m m i g r a t i o n of juvenile males than females, a n d this was more p r o n o u n c e d in the spring t h a n in the a u t u m n , A l t h o u g h m e a n lengths of residence were less t h a n 10 weeks, we were ultimately concerned with the n u m b e r of animals t h a t remained a n d bred in
their same h o m e range from one breeding season to the next. O n average, 20% of adult males and females a n d juvenile females r e m a i n e d a n d bred in the same h o m e range in subsequent breeding seasons (Table III). F r o m A u g u s t 1984 to spring 1986, only five of 101 ( 5 % ) j u v e n i l e males reached sexual m a t u r i t y a n d bred o n their natal h o m e ranges. F r o m spring to a u t u m n 1986, however, nine o f 83 (11%) juvenile males remained in their natal h o m e ranges. Six of these nine males were from one grid. Using the electrophoresis radionuclide technique we were able to identify the relationship (or lack thereof) between m o t h e r s a n d potential fathers in 135 matings. The radionuclide technique served to pair m o t h e r s a n d offspring. Potential
460
Animal Behaviour, 36, 2 Treble IV. The number of behavioural trials between adult and juvenile P. leucopus in which adult aggression, no aggression and non-aggressivecontact were exhibited Adult No Non-aggressive N aggression aggression contact 1985 Adult-juvenile males Adult-juvenile females
31 19
8 2
23 17
24 16
1986 Adult malesjuvenile males 18 Adult females~uvenilemales 14
5 2
13 12
9 7
All ;(2 between years and sexes were less than 2.90, df= 1, P>0.05.
fathers were assumed to be those males present at (SD~---1-3, N = 13) aggressive acts occurred per 5the approximate time of conception. Electrophore- rain trial and usually did not result in retreat by the tic analysis was conducted on these family group- juvenile. Non-aggressive contact occurred in 80% ings. Allele frequencies of the nine polymorphic and 50% of the trials in 1985 and 1986, respectively. loci used in this study are given in Table I. In five Animals frequently avoided each other, but over cases, daughters bred within home ranges of their 70% of the trials ended with no aggression. Adult fathers and in one case a sexually mature son's females treated juvenile males and females simihome range overlapped that of his mother when larly. Adult females exhibited aggression towards she became pregnant. In two cases the daughters' juvenile females in two of 19 ( l l % ) trials and litters were sired by someone other than their towards juvenile males in two of 14 (14%) trials. fathers. One female was FS at the ADA locus and Most adult-juvenile interactions were amicable and there was little evidence that adults were her offspring was SS. The female's father was F F and therefore he could not have sired the offspring. aggressively excluding juveniles. In the second case, the mother was MS at the ADA locus and her offspring was MM. The female's father was SS and could not have sired the Dispersal with Respect to the Social Environment By mapping home ranges of adult males, offspring. In three cases we were not able to reject the father as a possible mate. In the mother-son mothers, sons and daughters, we were able to case, the mother's litter was not sired by her son. determine the social environment of juveniles at the The mother and her son were FS at the NASA time of their disappearance (presumed dispersal). locus and the offspring from her second litter were The mean lengths of residence of sons did not differ MS. The father of the second litter would have to significantly whether they were living in the preshave had the M allele at the NASA locus. There- ence of an adult male (5.6 weeks, N = 16), their fore, the son could not have sired his mother's mothers or sisters (2.8 weeks, N = I 1), adult males second litter. Consequently, only three of 135 and their mothers or sisters (3.3 weeks, N=43), or (2-2%) matings involved possible parent-offspring in exclusive home ranges (4.3 weeks, N = 9 ; all Mann Whitney U-tests between all combinations inbreeding. No brothers and sisters out of 360 that were identified remained in their natal home ranges z's< 1-77, P>0.5). The mean length of residence and were involved in inbreeding. for sons was shorter when mothers or sisters remained in the natal home ranges, but this difference was not significant. The number of sons Adult-Juvenile Behaviour that remained on grid 3 (adult-male removal grid) Resident adult males exhibited aggression to- and control grids 8 and 9 in 1986 for less than or wards juvenile males in eight of 31 (26%) trials in greater than 2 weeks did not differ significantly 1985 and five of 18 (28%) trials in 1986 (Table IV). (Z2=0.5, dr=2, P>0-5; Table V). The number of In those trials involving aggression, a mean of 2.4 sons that disappeared before and after their
Wolff et al.: Dispersal in white-footed mice
461
Table V. The number of sons and daughters that disappeared before and after their mothers disappeared, and that remained in their maternal home ranges for less than or more than 2 weeks in 1986
Sex
Grid no.
Remained Disappeared before Disappeared after mother mother Less than More than disappeared* disappeared* 2 weekst 2 weekst
Sons
3 8 9 Allgrids
9 3 6 18
6 12 2 20
8 12 6 26
11 11 8 30
Daughters
3 8 9 Allgrids
9 1 3 13
3 10 4 17
11 4 3 18
4 11 13 28
* Mothers and offspring that disappeared at the same time and offspring that did not disperse were excluded from the analysis. t Animals that were on the edge of the grids were excluded from the analysis.
mothers disappeared in 1986 were 18 and 20, respectively, and did not differ significantly from the number of daughters that disappeared before (13) and after (17) their mothers disappeared (X2= 0.12, dr= 1, P > 0.5). The number of sons that remained on grid 3 from spring to autumn 1986 was one of 25 (4%), whereas the numbers that remained on control grids 8 and 9 were six of 27 (22%) and two of 31 (6%), respectively (Z2=5-54, d f = l , P < 0 ' 0 5 ) . This is not as expected if it is assumed that adult males are the cause of dispersal in juvenile males. More sons remained on control grid 8 in the presence of adult males than remained on grid 3 in the absence of adult males. It is interesting to note, however, that only one mother remained on grid 8 during juvenile recruitment. The number of daughters that remained on grids 8 and 9 for more than 2 weeks in 1986 was significantly greater than the number that remained on grid 3. Eleven of 15 (73%) daughters disappeared from grid 3 in less than 2 weeks compared to seven of 31 (23%) on grids 8 and 9 (Z2=10-8, df=2, P < 0 . 0 0 1 ; Table V) Thus, daughters showed a greater dispersal response to the absence of adult males on grid 3 than did sons. Mothers were found in nest boxes with their weaned, 12-15-g sons on 12 occasions. On two occasions the mothers were nursing second litters. Weaned brothers and sisters were found together eight times. Fathers and 15-g subadult sons were
observed together in nest boxes on three occasions. These results suggest that dispersal by sons is not 'forced' by adult males or female relatives. Sons may, however, leave 'voluntarily' if their mothers are present. However, this was not possible to test. In 13 of 14 cases where sons remained in their natal home ranges until the next breeding season, their mothers were gone, and in 17 of 18 cases where sons left their natal residence from grids 8 and 9 in less than 2 weeks (Table V), their mothers were still present.
Reproductive Success of Grid-born Animals and Immigrants The reproductive success of native, grid-born females did not differ significantly from that of immigrants. O f 306 females that were pregnant or lactating, 25 were native, grid-born animals, 215 were immigrants, and 66 were present on the grids when the project started and were of unknown origin. All 25 daughters that remained in their natal home ranges became pregnant, but only 13 (52%) successfully weaned at least one offspring. The weaning success rate of immigrant females was 57% (122 of215; Z2=0.12, df= 1, P > 0.5). Thus, of the 135 reproductively successful females from spring 1985 to autumn 1986 in which we knew the origin of the mothers, 10% (13 of 135) of the litters were borne by natal residents and 90% (122 of 135)
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Animal Behaviour, 36, 2
were borne by immigrants. Of all the litters, 4% (5 of 135) were sired by natal residents and 96% by immigrants.
DISCUSSION A considerable amount of dispersal occurs in P. leucopus, with approximately 80% of the population consisting of new immigrants each breeding season. Dispersal occurred among all ages in both sexes, but was most pronounced among juvenile males. Similar dispersal patterns occurred at moderate densities in 1985 and at high densities in 1986, except that fewer juvenile males dispersed in 1986. The mean lengths of residencies of adults and juveniles in this study were similar to those in 1984 (Wolff& Lundy 1985) and those from high densities in 1981 and low densities in 1983 (Wolff 1985a, 1986). The sex-bias of immigrants was not as obvious in autumn because family units tend to stay together in late autumn and early winter (Howard 1949; King 1983; Wolff& Durr 1986). By the following spring, however, most sons had dispersed from their natal home ranges. The lowest rates of juvenile male dispersal were at the highest densities in 1981 and in 1986. Juvenile males may remain in their natal home ranges at high densities because of the difficulty in colonizing saturated habitats. In this case, resident adult males would not force dispersal of their sons, but their presence could inhibit colonization by immigrants. Similar dispersal patterns occur in Microtus montanus where juveniles disperse at low densities, but remain in their natal home ranges at high densities and form extended family units (Jannett 1978). Dispersal of juvenile males is well-documented in Peromyscus (Howard 1949; Fairbairn 1978a, b; Krohne et al. 1984; Adler & Tamarin 1985; Wolff& Lundy 1985; Goundie & Vessey 1986). Several studies have suggested that dispersal of juvenile males is 'forced' by aggressive adult males (Sadleir 1965; Healey 1967; Pettigrew & Sadleir 1974; van Horne 1981), but the experimental results in this study do not support this hypothesis. Adult males were not aggressive towards juvenile males, and juvenile males dispersed from adult-male removal grids at the same rate as on control grids in the presence of adult males. We were not able to correlate juvenile male dispersal with the presence or absence of adult males. Juvenile males seemed to disperse irrespective of
their social environment, but sons were less likely to remain in their natal home ranges if their mothers were present. Only 14 of 184 sons remained in their natal home ranges until the next breeding season and in 13 of these cases their mothers were gone. The remaining 170 sons dispersed prior to the next breeding season whether or not their mothers were present. No brothers and sisters grew up together in their maternal home range. The six sons that remained in their natal home ranges on grid 8 until the next breeding season in 1986 did so in the absence of their mothers. Thus, the presence of a mother, or perhaps sister, and not males, may be the proximate stimulus for dispersal of juvenile males. Cockburn et al. (1985) found that in Antechinus spp. sons were forced by their mothers to disperse. Dispersal by juvenile Antechinus was not influenced by adult males, who die after breeding. We did not examine aggression between mothers and sons in this study, but the occurrence of mothers and sons together in nest boxes (see also Howard 1949; Wolff & Durr 1986) suggests that mothers do not aggressively exclude their sons. These results agree with those of Halpin (1981), Nadeau et al. (1981), King (1983) and Krohne et al. (1984) who concluded that juvenile males were not driven to disperse by their parents or other resident adults. Of these females, 20% remained in their natal home ranges and 80% dispersed (or disappeared). We were not able to determine why some females dispersed and others did not, but daughters were not negatively influenced by the presence of their mothers. The daughters that remained in their natal home ranges did so whether or not their mothers were present. The high dispersal rate of juvenile females on the adult-male removal grid suggests that females may seek home ranges that are occupied by adult males. Alternatively, females may have been avoiding the relatively high density of females; however, this did not occur on control grids with comparable densities of females. This finding was unexpected and requires further experimental study with replication. The dispersal of sons and the generally high turnover rate of the daughters and adults kept inbreeding below 3%. This is within the range of inbreeding reported for other natural populations (0 6%; Rails et al. 1986). Howard (1949) estimated inbreeding among P. maniculatus to be between 4% and 10%. This was based on presumed father-
Wolff et al.: Dispersal in white-footed mice daughter associations in nest boxes. In our study, we found that father-daughter associations did not necessarily mean inbreeding. Two of five fatherdaughter pairs did not mate, and the other three were uncertain. Grau (1982) found that P. leueopus recognize kin and may avoid mating with relatives. This may work for mothers and sons, and brothers and sisters, but, due to multiple inseminations (Baccus & Wolff, unpublished data) and the lack of paternal care, it is unlikely that fathers will recognize their daughters. The dispersal pattern and general mixing of the population between spring and autumn breeding seasons (approximately 90 days) is apparently sufficient to keep inbreeding at a minimum. Our data support the inbreeding avoidance hypothesis for male-biased dispersal (Packer 1979, 1985; Wolff & Lundy 1985; Harvey & R a l l s 1986) and not the reproductive competition hypothesis (Moore & Ali 1984). Haigh (1983a) demonstrated the detrimental effects of inbreeding in Peromyscus and Hill (1974), Dewsbury (1982), Haigh (1983b), Terman (1984) and Haigh et al. (1985) showed that the presence of relatives inhibits sexual maturation. Thus some mechanism by which weaned young separate from their parents and siblings would ensure the earliest onset of sexual maturation while at the same time prevent close inbreeding. Dispersal in Peromyscus may be associated in part with searching for mates (Fairbairn 1978a; Nadeau et al. 1981; King 1983), but this does not explain why juvenile males would disperse from a 3-ha grid that contained approximately 100 females and no adult males. Also, the juvenile males dispersed 60-90 days before they would have the opportunity to mate. Reproductive competition might, however, play a secondary role in dispersal of juvenile males by inhibiting colonization at high densities (Wolff 1985b). The mating system of P. leucopus ranges from polygyny and promiscuity to facultative monogamy (Wolff, in press). Therefore it is difficult to test the predictions of Dobson's (1982) and Liberg & Schantz's (1986) models. Female P. leucopus defend resources (food and their young from infanticide), and males defend females (Wolff 1985b, in press). Females have lower dispersal rates than males and they disperse shorter distances (Goundie & Vessey 1986). These results are compatible with the models of Greenwood (1980), Dobson (1982) and Liberg & Schantz (1986). However, the data parsimoniously support
463
inbreeding avoidance as the ultimate causation for sex-biased dispersal. Juvenile males appear to be preprogrammed to disperse independently of density or their social environment. Adult Peromyscus tended to remain in the same home range during the breeding season, and disperse just before or just after the breeding season (Howard 1949; King 1983; Krohne & Miner 1985; Wolff 1985a). The lengths of residence for adult males and females are similar (see also Wolff 1986), but it is interesting to note the degree of dispersal of pregnant and post-lactating females. Post-weaning dispersal apparently provides living space for daughters who inherit their maternal home ranges (Wolff & Lundy 1985), but the adaptive significance of leaving an established home range just prior to giving birth is unclear. Some of the 48 females that were pregnant when they disappeared probably died, but 23 pregnant females immigrated to the grids. These immigrating females may have made preliminary exploratory movements and found suitable vacant habitat for colonizing. Peromyseus, regardless of reproductive condition, frequently switch nest sites (Howard 1949; Wolff & Hurlbutt 1982; Wolff & Durr 1986), probably to reduce the chances that a predator will locate them. Dispersal of pregnant females may be as much a response to leaving a previous home range to their first litters, as it is to finding a new nest site. We do not know whether preparturition dispersal is more common among multiparous females than primiparous females. In this study the reproductive success of immigrants was similar to that of residents, so we have no evidence for a decrease in fitness for dispersing compared to non-dispersing females.
ACKNOWLEDGMENTS We thank J. Maldonado, S. Graves and M. Maxey for their assistance in the field and with the electrophoresis. J. Cranford provided stimulating discussion on the subject, and D. Krohne, D. Fairbairn and one anonymous reviewer made helpful comments on the manuscript. This work was supported by The Theodore Roosevelt Memorial Fund, The American Museum of Natural History, the Graduate Program at Virginia Polytechnic Institute and State University, and N S F Grant 83-06619. This paper is dedicated to Frank A. Pitelka.
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REFERENCES Adler, G. H. & Tamarin, R. H. 1985. Dispersal of whitefooted mice, Peromyscus leucopus, in low-density island and mainland populations. Can. Field Nat., 99, 331 336. Ayala, F. J., Powell, F. J., Tracey. M. L., Mourac, C. A. & Perez-Salas, S. 1972. Enzyme variability in the Drosophila willistoni group. IV. Genetic variation in natural populations of Drosophila willistoni. Genet&s, 70, 113139. Ballou, J. & Rails, K. 1982. Inbreeding and juvenile mortality in small populations of ungulates: a detailed analysis. Biol. Conserv., 24, 239-272. Brody, A. K. & Armitage, K. B. 1985. The effects of adult removal on dispersal of yearling yellow-bellied marmots. Can. J. ZooL, 63, 2560 2564. Chesser, R. K. & Ryman, N. 1986. Inbreeding as a strategy in subdivided populations. Evolution, 40, 616624. Cockburn, A., Scott, M. P. & Scotts, D. J. 1985. Inbreeding avoidance and male-biased dispersal in Antechinus spp. (Marsupialia: Dasyuridae). Anim. Behav., 33, 908-915. Connor, R. J. & Bellucci, M. J. 1979. Natural selection resisting inbreeding depression in captive wild housemice (Mus musculus). Evolution, 33, 929-940. Dewsbury, D. A. 1982. Avoidance of incestuous breeding between siblings in two species of Peromyscus mice. Biol. Behav., 7, 157-169. Dobson, F. S. 1982. Competition for mates and predominant juvenile male dispersal in mammals. Anim. Behav., 30, 1183 1192. Fairbairn, D. J. 1978a. Dispersal of deermice, Peromyscus manieulalus: proximal causes and effects on fitness. Oecologia (Berl.), 32, 171-193. Fairbairn, D. J. 1978b. Behaviour of dispersing deer mice (Peromyscus maniculatus). Behav. Ecol. Sociobiol., 3, 265-282. Foltz, D. W. 1981. Genetic evidence for long-term monogamy in a small rodent, Peromyscus polionotus. Am. Nat., 117, 665-675. Gaines, M. S. & McClenaghan, L. R., Jr. 1980. Dispersal in small mammals. A. Rev. Ecol. Syst., 11, 163-196. Goundie, T. R. & Vessey, S. H. 1986. Survival and dispersal of young white-footed mice born in nest boxes. J. Mammal., 67, 53-60. Grau, H. J. 1982. Kin recognition in white-footed deermice (Peromyscus leucopus). Anim. Behav., 30, 497-505. Greenwood, P. J. 1980. Mating systems, philopatry and dispersal in birds and mammals. Anita. Behav., 28,
1140-1162. Haigh, G. R. 1983a. The effects of inbreeding and social factors on the reproduction of young female Peromyscus maniculatus bairdii. J. Mammal., 64, 48 54. Haigh, G. R. 1983b. Reproductive inhibition and recovery in young female Peromyscus leucopus. J. Mammal., 64, 706. Haigh, G. R., Lounsburg, D. A. & Gordon, T. G. 1985. Pheromone induced reproductive inhibition in young female Peromyscus leucopus. Biol. Reprod., 33, 271276.
Halpin, Z. T. 1981. Adult-young interactions in island and mainland populations of the deermouse, Peromyscus maniculatus. Oecologia (Berl.), 51,419~,25. Harvey, P. H. &Ralls, K. 1986. Do animals avoid incest? Nature, Lond., 320, 575-576. Healey, M. C. 1967. Aggression and self-regulation of population size in deermice. Ecology, 48, 377-392. Hilborn, R., Redfield, J. A. & Krebs, C. J. 1976. On the reliability of enumeration for mark and recapture census of voles. Can. J. Zool., 54, 1019-1024. Hill, J. L. 1974. Peromyscus." effects of early pairing on reproduction. Science, N.Y., 186, 1042-1044. Hoogland, J. L. 1982. Prairie dogs avoid extreme inbreeding. Science, N.Y., 215, 1639 1641. van Home, B. 1981. Niches of adult and juvenile deer mice Peromyscus maniculatus in seral stages of coniferous forest. Ecology, 63, 922-1003. Howard, W. E. 1949. Dispersal, amount of inbreeding, and longevity in a local population of prairie deermice on the George Reserve southern Michigan. Contr. Lab, Vetebr. Biol. Univ. Mich., 43, 1 52. Jannett, F. J., Jr. 1978. The density-dependent formation of extended maternal-families of the montane vole, Microtus montanus nanus. Behav. Ecol. Sociobiol., 3, 245 263. King, J. A. 1983. Seasonal dispersal in a seminatural population of Peromyscus maniculatus. Can. J. Zool., 61, 2740-2750. Krohne, D. T., Dubbs, D. A. & Baccus, R. 1984. An analysis of dispersal in an unmanipulated population of Peromyscus leucopus. Am. Midl. Nat., 112, 146-156. Krohne, D. T. & Miner, M. S. 1985. Removal trapping studies of dispersal in Peromyscus leucopus. Can. J. Zool., 63, 71-75. Liberg, O. & Schantz, T. V. 1986. Sex-biased philopatry and dispersal in birds and mammals: the Oedipus hypothesis. Am. Nat., 126, 129-135. Lidicker, W. Z., Jr. 1985. Dispersal. In: Biology of New World Microtus (Ed. by R. H. Tamarin), pp. 420-454. Lawrence, Kansas: Allen Press. Moore, J. & Ali, R. 1984. Are dispersal and inbreeding avoidance related? Anim. Behav., 32, 94-I 12. Nadeau, J. H., Lombardi, J. M. & Tamarin, R. H. 1981. Population structure and dispersal of Peromyscus leucopus on Muskeget Island. Can. J. Zool., 59, 793799. Nicholson, A. J. 1941. The homes and social habits of the wood-mouse (Peromyscus leucopus noveboracensis) in southern Michigan. Am. Midl. Nat., 25, 196-223. Packer, C. 1979. Intergroup transfer and inbreeding avoidance in Papio anubis. Anita. Behav., 27, 1-36. Packer, C. 1985. Dispersal and inbreeding avoidance. Anita. Behav., 33, 676-678. Pettigrew, B. G. & Sadleir, R. M. F. S. 1974. The ecology of the deermice, Peromyscus maniculatus, in a coastal coniferous forest. I. Population dynamics. Can. J. Zool., 52, 107 118. Rails, K., Brugger, K. & Ballou, J. 1979. Inbreeding and juvenile mortality in small populations of ungulates. Science, N. Y., 206, 1101-1103. Rails, K., Harvey, P. H. & Lyles, A. M. 1986. Inbreeding in natural populations of birds and mammals. In: Conservation Biology (Ed. by M. E. Soule'), pp. 35-56.
Wolff et al.: Dispersal in white-footed mice Sunderland, Massachusetts: Sinauer. Sadleir, R. M. F. S. 1965. The relationship between agonistic behaviour and population changes in the deer mouse, Peromyscus maniculatus. J. Anim. Ecol., 34, 331-352. Selander, R. K., Smith, M. H., Yang, S. Y., Johnson, M. E. & Gentry, J. B. 1971. Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse. Studies in genetics. Univ. Texas Publ., 6, 84-90. Shields, W. M. 1982. Philopatrv, Inbreeding, and the Evolution of Sex. Albany: State University of New York Press. Smith, R. H. 1979. On selection for inbreeding in polygynous animals. Heredity, 43, 205 211. Stenseth, N. C. 1983. Causes and consequences of dispersal in small mammals. In: The Ecology of Animal Movement (Ed. by I. R. Swingland & P. J. Greenwood), pp. 63-101. Cambridge: Oxford University Press. Tamarin, R. H., Sheridan, M. & Levy, C. H. 1983. Determining matrilineal kinship in natural populations of rodents using radionuclides. Can. J. Zool., 61,271 274. Terman, C. R. 1984. Sexual maturation of male and female white-footed mice (Peromyscus leucopus noveboracensis): influence of urine and physical contact with adults. J. Mammal., 65, 97 102. Wolff, J. O. 1985a. Comparative population ecology Peromyscus leucopus and P. maniculatus. Can. J. Zool.,
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63, 1548-1555. Wolff, J. O. 1985b. The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and P. maniculatus. Can. J. Zool., 63, 2657-2662. Wolff, J. O. 1985c. Maternal aggression as a deterrent to infanticide in Peromyscus leucopus and P. maniculatus. Anita. Behav., 33, 117-123. Wolff, J. O. 1986. Life history strategies of white-footed mice (Peromyscus leucopus). Virg. J. Sci., 37, 208 220. Wolff, J. O. In press. Social behavior. In: Biology of Peromyscus 1968-1985 (Ed. by G. L. Kirkland, Jr & J. N. Layne). Lawrence, Kansas: Allen Press. Wolff, J. O. & Durr, D. S. 1986. Winter nesting behavior of Peromyscus leucopus and Peromyscus maniculatus. J. Mammal., 67, 409-411. Wolff, J. O. & Hurlbutt, B. 1982. Day refuges of Peromyscus leucopus and P. maniculatus. J. Mammal., 63, 666-668. Wolff, J. O. & Lundy, K. I. 1985. Intra-familial dispersion patterns in white-footed mice, Peromyscus leucopus. Behav. Ecol. Sociobiol., 17, 831 834. Wolff, J. O., Freeberg, M. H. & Dueser, R. D. 1983. Interspecific territoriality in two sympatric species of Peromyscus (Rodentia: Cricetidae). Behav. Ecol. Sociobiol., 12, 237 242.
(Received 30 January 1987; revised 4 May 1987; MS. number: ,~4959)
Dispersal, inbreeding avoidance and reproductive success in white-footed mice J E R R Y O. W O L F F * , K A T H A R I N E
I. L U N D Y t
& R A M O N E BACCUS:~
*Biology Department, Villanova University, Villanova, PA 19085, U.S.A. t312 New Hackensack Rd., Poughkeepsie, N Y 12603, U.S.A. ~Biology Department, Berry College, Mount Berry, GA 30149, U.S.A.
Abstract. The dispersion pattern of 360 juvenile white-footed mice, Peromyscus leucopus, from 158 matings was monitored to determine whether dispersal was sufficient to prevent close inbreeding. Dispersal was male-biased with 20% of the daughters remaining in their natal home ranges. Dispersal of sons was not 'forced' by adult males, but may have been influenced by the presence of their mothers. One mother-son and five father-daughter pairs had overlapping home ranges during the breeding season, but the maximum number of matings among close relatives was three of 135 (2.2%). Dispersal of juvenile males was sufficient to keep close inbreeding at a minimum. Dispersal did not result from reproductive competition. Pregnant and post-lactating females frequently moved to new home ranges. The reproductive success of immigrants was the same as that of natal residents.
Considerable controversy exists over the proximate and ultimate causes of sex-biased dispersal (Greenwood 1980; Dobson 1982; Moore & Ali 1984; Packer 1985; Harvey & Rails 1986; Liberg & Schantz 1986). Greenwood (1980) proposed that in mammals, females compete for resources and therefore dispersal should be male-biased. Dobson (1982) argued that dispersal is related to the type of mating system and should be male-biased among polygynous and promiscuous mammals and show no bias in monogamous species. Liberg & Schantz (1986) used the reverse approach and concluded that natal philopatry should be female-biased in polygynous and promiscuous mammals. Packer (1979), Krohne et al. (1984), Wolff& Lundy (1985), Harvey & Rails (1986) and others argue that malebiased dispersal in mammals has evolved as a mechanism to prevent inbreeding with the more philopatric females. Moore & Ali (1984), on the other hand, countered that juvenile males disperse not to prevent inbreeding, but to reduce competition with resident adult males (but see Packer 1985). Harvey & Rails (1986) summarized these arguments and concluded that inbreeding avoidance was the most parsimonious explanation for male-biased dispersal among mammals. These results have been supported by a number of field studies on, among others, marmots (Marmota flaviventris; Brody & Armitage 1985), prairie dogs (Cynomys ludovicianus; Hoogland 1982) and the marsupial Antechinus (Cockburn et al. 1985). The deleterious effects of inbreeding are well-known
(Connor & Bellucci 1979; Rails et al. 1979; Ballou & Rails 1982; Haigh 1983a; Ralls et al. 1986; but see Smith 1979; Shields 1982; Chesser & Ryman 1986, for situations where inbreeding may be advantageous). Thus, sex-biased dispersal would be an adaptive mechanism to separate relatives prior to mating. Dispersal is common among small mammals and apparently serves a number of functions (see Gaines & McClenaghan 1980; Stenseth 1983; Lidicker 1985, for reviews). Dispersal that is dependent on density has been suggested in a number of studies, but Krohne et al. (1984), Nadeau et al. (1981), Adler & Tamarin (1985) and Wolff & Lundy (1985) concluded that dispersal among Peromyscus is more closely associated with mating behaviour than density per se. Wolff & Lundy (1985) found that juvenile male P. leucopus dispersed whereas juvenile females were more philopatric and inherited their maternal home range (see also Nicholson 1941). Dispersal of sons prevented mother-son and brother-sister matings, but daughters often had home ranges overlapping those of males who could have been their fathers. Wolff & Lundy concluded that mother-son and brother-sister matings were unlikely, but they could not reject the possibility of father-daughter matings, In an earlier study with P. maniculatus in nest boxes, Howard (1949) frequently found fathers and daughters together and concluded that inbreeding may be as high as 10%. Goundie & Vessey (1986) also found that home ranges of
456
Wolff et al.: Dispersal in white-footed mice
457
Table I. Locus designations and allele frequencies for nine polymorphic presumptive loci from blood tissue found in Peromyseus leucopus Allele designation Isozyme Catalase (CAT) Carbonic anhydrase (CA) Adenosine deaminase (ADA) 6-Phosphogluconatedehydrogenase(6-PGD) Phosphoglucose isomerase (PGI) Naphthyl-AS-acetate esterase (NASA) Purine nucleoside phosphorylase (NP) Post-albumin (P-ALB) Transferrin(TRF)
siblings and of parents and offspring overlapped in a 2-ha woodlot population of P. leucopus and suggested the possibility of inbreeding. In this study we used the radionuclide-electrophoresis technique (Tamarin et al. 1983) to identify mothers, potential fathers and offspring of whitefooted mice, Peromyscus leucopus, and followed their dispersal and dispersion pattern during subsequent breeding seasons to measure the incidence of close inbreeding (parent-offspring or siblings). We also examined the effects of density, adult aggression, and the presence of adult males or female relatives on dispersal of juvenile males. These results were interpreted with respect to proximate and ultimate causation for sex-biased dispersal. Lastly, the reproductive success of natal residents (animals born on the study site) was compared with that of immigrants.
M A T E R I A L S AND M E T H O D S The study was conducted at the Mountain Lake Biological Station in Giles County, southwestern Virginia, U.S.A. (37°10'N, 80°30'W). The Station is at an elevation of 1200 m in the Allegheny Mountains in an oak-hickory-maple forest scattered with rhododendron, Rhododendron sp., thickets and an understory of ferns (primarily Osmunda spp.) and blueberry, Vaccinium spp. The behavioural ecology of Peromyscus in this region is well-known (Wolff et al. 1983; Wolff 1985a, b, c, 1986). Home ranges of males and females overlap, but are exclusive within each sex. The mating system ranges from promiscuity to facultative monogamy. Two breeding seasons occur each year,
F
M
0.101 0.011 0.008 0-461 0.433
0.488 0.608 0.416 0.989 0.992 0.126 0.556 0.975 0.943
0.029
S
S'
0.512 0.392 0.474 0.009 0.400 0.013 0.011 0.025 0.043
one in April-June and the other in SeptemberNovember. Spring-born animals breed in the autumn and autumn-born animals breed the following spring. Four 3-ha live-trapping grids were established in similar habitat within 500 m of the Station. Each grid consisted of 196 trap stations in an array of 14 x 14 with 12.5 m spacing. One large Sherman live-trap baited with solid shortening was placed at each station. Animals were trapped for 2 or 3 consecutive days at intervals of 2-3 weeks from August through November 1984, March through November 1985, and March through July 1986, and a final census was conducted in October 1986. Only three of the four grids (3, 8 and 9) were trapped in 1986. The study included three autumn and two spring breeding seasons. Animals were ear-tagged for permanent identification, and species, sex, age, weight, reproductive condition and trap locations were recorded. Females were recorded as pregnant if they had swollen abdomens and lactating if they had large nipples. Males were recorded as having scrotal or abdominal testes. A radionuclide technique was used to determine matrilineal relationships (Tamarin et al. 1983) and an electrophoretic paternity-exclusionanalysis was used to determine putative fathers (Foltz 1981). All pregnant or lactating females were injected with 15 ~Ci of iron (59Fe), strontium (8SSr), selenium (7SSe), zinc (6SZn), caesium (137Cs), manganese (lS4Mn), or chromium (51Cr) diluted in 0.5-ml saline solution (Wolff & Lundy 1985). The isotopes transferred to the young in utero and through the milk. Different isotope combinations were given to animals on the same grid. All juveniles were scanned on a multi-channel ion-isotope analyser
458
Animal Behaviour, 36, 2
when they were first captured. Each radionuclide had unique spectral peaks so juveniles could be accurately assigned to their mothers and siblings. Approximately 1 ml of blood was collected from the orbital sinus of most animals. A paternityexclusion analysis was conducted by analysing nine polymorphic presumptive loci found in plasma and red blood cells using standard techniques for starch-gel electrophoresis (Table I). Tris citrate buffer pH 7.0 was used for CAT, CA, ADA, and 6PGD (Ayala et al. 1972), and lithium hydroxide was used for PGI, NASA, NP, P-ALB and T R F (Selander et al. 1971). Behavioural trials were conducted between adults and juveniles within the home range of the adults using the technique of Wolffet al. (1983) and Wolff(1985b). In each trial an adult (weighing 18 g or more and sexually mature) and a juvenile (weighing less than 18 g and not reproductive) were placed in a clear, open-bottom, Plexiglas cylinder 32 cm in diameter and 48 cm high. Each trial lasted 5 rain and three behaviours were recorded. (I) Aggression: an attack or offensive approach in which one animal attempts to displace the other, resulting in a retreat, submission, or counter attack. (2) Avoidance: one animal avoids and moves away from the other animal just because of its presence not because of any aggressive behaviour. (3) Non-aggressive contact: touching such as sniffing, crawling over each other, or huddling that does not elicit an aggressive response. Fifteen wooden nest boxes (Wolff& Durr 1986) were placed between 1 and 2 m in trees on each grid and checked periodically throughout the study. Sex, tag number, weight, and reproductive condition were recorded on nest box occupants. During the juvenile recruitment period of 15 May through 15 June 1986, all adult males were removed from grid 3. This was done to see whether juvenile males would remain in their natal home ranges if no adult males were present. Home ranges were estimated by drawing a minimum-area polygon around the trap stations where resident animals were caught three or 'more times over at least a 2-week period (Wolff 1985b). We could not separate dispersal from death in this study, but we have no evidence of sex differences in mortality among Peromyseus (Wolff & Lundy 1985). Consequently, dispersal will refer to all animals that disappeared from the grids, assuming that equal proportions of each sex died.
RESULTS
Population Density The population density (minimum number alive) of P. leucopus ranged from 15 to 20 animals/ha in 1984 and 1985, and reached a peak of 38 animals/ ha in June 1986. At any time, an additional 5-10 animals/ha of P. maniculatus occurred syntopically with P. leucopus (Wolff et al. 1983; Wolff 1985b). Trappability (Hilborn et al. 1976) was 94%.
Pregnancy and Weaning Rates A total of 306 pregnant or lactating females were caught on grids from August 1984 through June 1986. Of these females, 221 remained in residence longer than 4 weeks; long enough to wean a litter. These 221 females produced 243 pregnancies; however, only 151 females successfully weaned 158 litters. We identified 184 sons and 176 daughters of these 151 females. The mean number of weaned offspring per successful litter (at least one young weaned) was 2.4. Mean litter size for P. leucopus is 3.4 (Wolff 1986) so weaning rate was 70%. An additional 55 sons and 47 daughters were found in nest boxes or had isotopes indicating they were born on the grids, but they could not be accurately assigned to any mother. Of those females that successfully weaned at least one young, 27 disappeared after a 3-week lactation period, 84 stayed in their same home range after weaning, and 40 were on the edge of grids and their fate could not be determined. Fortyeight females disappeared while pregnant and 23 females immigrated while they were pregnant and were within a couple of days of parturition.
Residency, Dispersal and Inbreeding The mean length of residence was determined for 246 animals that were initially caught on the grids from April through June 1985. Animals on the edge of grids were excluded from the analysis. The mean lengths of residence were not significantly different for adult males (9-2 weeks+0-70 so, N=77) and females (9.2 weeks___0-74 so, N = 68; Mann-Whitney U-test, z=0-076, P=0-94), but they were different for juvenile males (4.4 weeks+0.49 so, N = 54), and juvenile females (7.5 weeks+ 1-00 SD, N=47; z=2.012, P=0'044). The number of juvenile males and females moving onto grids during the May-July 1985
Wolff et al.: Dispersal in white-#ooted mice
459
Table lI. The number of juvenile male and female P. leucopus that
immigrated to open grids during three breeding seasons Spring 1 9 8 5 Grid no. Males Females 3 8 9 16 Total
18 18 31 16 83
8* 7* 11" 14 40*
Autumn 1985
Spring 1986
Males Females
Males Females
26 12 15 17 70
13" 14 19 24 70
45 38 23 -106
24* 24 22 -70*
* For differences between males and females for each grid and season )C~ >3.48, df= 1, P<0.05. Table I!I. The number and (percentage) of animals present on a grid in one breeding season that remained in their same home range until the subsequent breeding season
Age/sex Fathers Mothers Present in autumn 1984 Remained until spring 1985 Present in spring 1985 Remained untilautumn 1985 Present in autumn 1985 Remained until spring 1986 Present in spring 1986 Remaineduntilautumn 1986 Total All breeding seasons Next breeding seasons
Sons
Daughters
36 14 (39) 49 10 (20) 47 9 (19) 44 2 (5)*
23 8 (35) 41 8 (20) 28 7 (25) 59 8 (14)
24 1 (4) 54 2 (4) 23 2 (9) 83 9(ll)t
21 10 (48) 47 7 (15) 38 8 (21) 70 10 (14)
176 35 (20)
151 31 (21)
184 14 (8)
176 35 (20)
* All adult males were removed from grid 3. t Six of nine sons were on grid 8.
recruitment period was 83 a n d 40, respectively (Table II). W i t h a 1 : 1 sex ratio in the p o p u l a t i o n (Wolff 1986), these values were significantly different o n three o f four grids. Sex ratios of juvenile i m m i g r a n t s were similar o n three of four grids in a u t u m n 1985, with only grid 3 showing a significant influx o f males. In spring 1986, i m m i g r a t i o n favoured males o n two of three grids, b u t was significant only on grid 3. A l t h o u g h a considerable n u m b e r of females dispersed a n d immigrated, the general trend was for greater i m m i g r a t i o n of juvenile males than females, a n d this was more p r o n o u n c e d in the spring t h a n in the a u t u m n , A l t h o u g h m e a n lengths of residence were less t h a n 10 weeks, we were ultimately concerned with the n u m b e r of animals t h a t remained a n d bred in
their same h o m e range from one breeding season to the next. O n average, 20% of adult males and females a n d juvenile females r e m a i n e d a n d bred in the same h o m e range in subsequent breeding seasons (Table III). F r o m A u g u s t 1984 to spring 1986, only five of 101 ( 5 % ) j u v e n i l e males reached sexual m a t u r i t y a n d bred o n their natal h o m e ranges. F r o m spring to a u t u m n 1986, however, nine o f 83 (11%) juvenile males remained in their natal h o m e ranges. Six of these nine males were from one grid. Using the electrophoresis radionuclide technique we were able to identify the relationship (or lack thereof) between m o t h e r s a n d potential fathers in 135 matings. The radionuclide technique served to pair m o t h e r s a n d offspring. Potential
460
Animal Behaviour, 36, 2 Treble IV. The number of behavioural trials between adult and juvenile P. leucopus in which adult aggression, no aggression and non-aggressivecontact were exhibited Adult No Non-aggressive N aggression aggression contact 1985 Adult-juvenile males Adult-juvenile females
31 19
8 2
23 17
24 16
1986 Adult malesjuvenile males 18 Adult females~uvenilemales 14
5 2
13 12
9 7
All ;(2 between years and sexes were less than 2.90, df= 1, P>0.05.
fathers were assumed to be those males present at (SD~---1-3, N = 13) aggressive acts occurred per 5the approximate time of conception. Electrophore- rain trial and usually did not result in retreat by the tic analysis was conducted on these family group- juvenile. Non-aggressive contact occurred in 80% ings. Allele frequencies of the nine polymorphic and 50% of the trials in 1985 and 1986, respectively. loci used in this study are given in Table I. In five Animals frequently avoided each other, but over cases, daughters bred within home ranges of their 70% of the trials ended with no aggression. Adult fathers and in one case a sexually mature son's females treated juvenile males and females simihome range overlapped that of his mother when larly. Adult females exhibited aggression towards she became pregnant. In two cases the daughters' juvenile females in two of 19 ( l l % ) trials and litters were sired by someone other than their towards juvenile males in two of 14 (14%) trials. fathers. One female was FS at the ADA locus and Most adult-juvenile interactions were amicable and there was little evidence that adults were her offspring was SS. The female's father was F F and therefore he could not have sired the offspring. aggressively excluding juveniles. In the second case, the mother was MS at the ADA locus and her offspring was MM. The female's father was SS and could not have sired the Dispersal with Respect to the Social Environment By mapping home ranges of adult males, offspring. In three cases we were not able to reject the father as a possible mate. In the mother-son mothers, sons and daughters, we were able to case, the mother's litter was not sired by her son. determine the social environment of juveniles at the The mother and her son were FS at the NASA time of their disappearance (presumed dispersal). locus and the offspring from her second litter were The mean lengths of residence of sons did not differ MS. The father of the second litter would have to significantly whether they were living in the preshave had the M allele at the NASA locus. There- ence of an adult male (5.6 weeks, N = 16), their fore, the son could not have sired his mother's mothers or sisters (2.8 weeks, N = I 1), adult males second litter. Consequently, only three of 135 and their mothers or sisters (3.3 weeks, N=43), or (2-2%) matings involved possible parent-offspring in exclusive home ranges (4.3 weeks, N = 9 ; all Mann Whitney U-tests between all combinations inbreeding. No brothers and sisters out of 360 that were identified remained in their natal home ranges z's< 1-77, P>0.5). The mean length of residence and were involved in inbreeding. for sons was shorter when mothers or sisters remained in the natal home ranges, but this difference was not significant. The number of sons Adult-Juvenile Behaviour that remained on grid 3 (adult-male removal grid) Resident adult males exhibited aggression to- and control grids 8 and 9 in 1986 for less than or wards juvenile males in eight of 31 (26%) trials in greater than 2 weeks did not differ significantly 1985 and five of 18 (28%) trials in 1986 (Table IV). (Z2=0.5, dr=2, P>0-5; Table V). The number of In those trials involving aggression, a mean of 2.4 sons that disappeared before and after their
Wolff et al.: Dispersal in white-footed mice
461
Table V. The number of sons and daughters that disappeared before and after their mothers disappeared, and that remained in their maternal home ranges for less than or more than 2 weeks in 1986
Sex
Grid no.
Remained Disappeared before Disappeared after mother mother Less than More than disappeared* disappeared* 2 weekst 2 weekst
Sons
3 8 9 Allgrids
9 3 6 18
6 12 2 20
8 12 6 26
11 11 8 30
Daughters
3 8 9 Allgrids
9 1 3 13
3 10 4 17
11 4 3 18
4 11 13 28
* Mothers and offspring that disappeared at the same time and offspring that did not disperse were excluded from the analysis. t Animals that were on the edge of the grids were excluded from the analysis.
mothers disappeared in 1986 were 18 and 20, respectively, and did not differ significantly from the number of daughters that disappeared before (13) and after (17) their mothers disappeared (X2= 0.12, dr= 1, P > 0.5). The number of sons that remained on grid 3 from spring to autumn 1986 was one of 25 (4%), whereas the numbers that remained on control grids 8 and 9 were six of 27 (22%) and two of 31 (6%), respectively (Z2=5-54, d f = l , P < 0 ' 0 5 ) . This is not as expected if it is assumed that adult males are the cause of dispersal in juvenile males. More sons remained on control grid 8 in the presence of adult males than remained on grid 3 in the absence of adult males. It is interesting to note, however, that only one mother remained on grid 8 during juvenile recruitment. The number of daughters that remained on grids 8 and 9 for more than 2 weeks in 1986 was significantly greater than the number that remained on grid 3. Eleven of 15 (73%) daughters disappeared from grid 3 in less than 2 weeks compared to seven of 31 (23%) on grids 8 and 9 (Z2=10-8, df=2, P < 0 . 0 0 1 ; Table V) Thus, daughters showed a greater dispersal response to the absence of adult males on grid 3 than did sons. Mothers were found in nest boxes with their weaned, 12-15-g sons on 12 occasions. On two occasions the mothers were nursing second litters. Weaned brothers and sisters were found together eight times. Fathers and 15-g subadult sons were
observed together in nest boxes on three occasions. These results suggest that dispersal by sons is not 'forced' by adult males or female relatives. Sons may, however, leave 'voluntarily' if their mothers are present. However, this was not possible to test. In 13 of 14 cases where sons remained in their natal home ranges until the next breeding season, their mothers were gone, and in 17 of 18 cases where sons left their natal residence from grids 8 and 9 in less than 2 weeks (Table V), their mothers were still present.
Reproductive Success of Grid-born Animals and Immigrants The reproductive success of native, grid-born females did not differ significantly from that of immigrants. O f 306 females that were pregnant or lactating, 25 were native, grid-born animals, 215 were immigrants, and 66 were present on the grids when the project started and were of unknown origin. All 25 daughters that remained in their natal home ranges became pregnant, but only 13 (52%) successfully weaned at least one offspring. The weaning success rate of immigrant females was 57% (122 of215; Z2=0.12, df= 1, P > 0.5). Thus, of the 135 reproductively successful females from spring 1985 to autumn 1986 in which we knew the origin of the mothers, 10% (13 of 135) of the litters were borne by natal residents and 90% (122 of 135)
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were borne by immigrants. Of all the litters, 4% (5 of 135) were sired by natal residents and 96% by immigrants.
DISCUSSION A considerable amount of dispersal occurs in P. leucopus, with approximately 80% of the population consisting of new immigrants each breeding season. Dispersal occurred among all ages in both sexes, but was most pronounced among juvenile males. Similar dispersal patterns occurred at moderate densities in 1985 and at high densities in 1986, except that fewer juvenile males dispersed in 1986. The mean lengths of residencies of adults and juveniles in this study were similar to those in 1984 (Wolff& Lundy 1985) and those from high densities in 1981 and low densities in 1983 (Wolff 1985a, 1986). The sex-bias of immigrants was not as obvious in autumn because family units tend to stay together in late autumn and early winter (Howard 1949; King 1983; Wolff& Durr 1986). By the following spring, however, most sons had dispersed from their natal home ranges. The lowest rates of juvenile male dispersal were at the highest densities in 1981 and in 1986. Juvenile males may remain in their natal home ranges at high densities because of the difficulty in colonizing saturated habitats. In this case, resident adult males would not force dispersal of their sons, but their presence could inhibit colonization by immigrants. Similar dispersal patterns occur in Microtus montanus where juveniles disperse at low densities, but remain in their natal home ranges at high densities and form extended family units (Jannett 1978). Dispersal of juvenile males is well-documented in Peromyscus (Howard 1949; Fairbairn 1978a, b; Krohne et al. 1984; Adler & Tamarin 1985; Wolff& Lundy 1985; Goundie & Vessey 1986). Several studies have suggested that dispersal of juvenile males is 'forced' by aggressive adult males (Sadleir 1965; Healey 1967; Pettigrew & Sadleir 1974; van Horne 1981), but the experimental results in this study do not support this hypothesis. Adult males were not aggressive towards juvenile males, and juvenile males dispersed from adult-male removal grids at the same rate as on control grids in the presence of adult males. We were not able to correlate juvenile male dispersal with the presence or absence of adult males. Juvenile males seemed to disperse irrespective of
their social environment, but sons were less likely to remain in their natal home ranges if their mothers were present. Only 14 of 184 sons remained in their natal home ranges until the next breeding season and in 13 of these cases their mothers were gone. The remaining 170 sons dispersed prior to the next breeding season whether or not their mothers were present. No brothers and sisters grew up together in their maternal home range. The six sons that remained in their natal home ranges on grid 8 until the next breeding season in 1986 did so in the absence of their mothers. Thus, the presence of a mother, or perhaps sister, and not males, may be the proximate stimulus for dispersal of juvenile males. Cockburn et al. (1985) found that in Antechinus spp. sons were forced by their mothers to disperse. Dispersal by juvenile Antechinus was not influenced by adult males, who die after breeding. We did not examine aggression between mothers and sons in this study, but the occurrence of mothers and sons together in nest boxes (see also Howard 1949; Wolff & Durr 1986) suggests that mothers do not aggressively exclude their sons. These results agree with those of Halpin (1981), Nadeau et al. (1981), King (1983) and Krohne et al. (1984) who concluded that juvenile males were not driven to disperse by their parents or other resident adults. Of these females, 20% remained in their natal home ranges and 80% dispersed (or disappeared). We were not able to determine why some females dispersed and others did not, but daughters were not negatively influenced by the presence of their mothers. The daughters that remained in their natal home ranges did so whether or not their mothers were present. The high dispersal rate of juvenile females on the adult-male removal grid suggests that females may seek home ranges that are occupied by adult males. Alternatively, females may have been avoiding the relatively high density of females; however, this did not occur on control grids with comparable densities of females. This finding was unexpected and requires further experimental study with replication. The dispersal of sons and the generally high turnover rate of the daughters and adults kept inbreeding below 3%. This is within the range of inbreeding reported for other natural populations (0 6%; Rails et al. 1986). Howard (1949) estimated inbreeding among P. maniculatus to be between 4% and 10%. This was based on presumed father-
Wolff et al.: Dispersal in white-footed mice daughter associations in nest boxes. In our study, we found that father-daughter associations did not necessarily mean inbreeding. Two of five fatherdaughter pairs did not mate, and the other three were uncertain. Grau (1982) found that P. leueopus recognize kin and may avoid mating with relatives. This may work for mothers and sons, and brothers and sisters, but, due to multiple inseminations (Baccus & Wolff, unpublished data) and the lack of paternal care, it is unlikely that fathers will recognize their daughters. The dispersal pattern and general mixing of the population between spring and autumn breeding seasons (approximately 90 days) is apparently sufficient to keep inbreeding at a minimum. Our data support the inbreeding avoidance hypothesis for male-biased dispersal (Packer 1979, 1985; Wolff & Lundy 1985; Harvey & R a l l s 1986) and not the reproductive competition hypothesis (Moore & Ali 1984). Haigh (1983a) demonstrated the detrimental effects of inbreeding in Peromyscus and Hill (1974), Dewsbury (1982), Haigh (1983b), Terman (1984) and Haigh et al. (1985) showed that the presence of relatives inhibits sexual maturation. Thus some mechanism by which weaned young separate from their parents and siblings would ensure the earliest onset of sexual maturation while at the same time prevent close inbreeding. Dispersal in Peromyscus may be associated in part with searching for mates (Fairbairn 1978a; Nadeau et al. 1981; King 1983), but this does not explain why juvenile males would disperse from a 3-ha grid that contained approximately 100 females and no adult males. Also, the juvenile males dispersed 60-90 days before they would have the opportunity to mate. Reproductive competition might, however, play a secondary role in dispersal of juvenile males by inhibiting colonization at high densities (Wolff 1985b). The mating system of P. leucopus ranges from polygyny and promiscuity to facultative monogamy (Wolff, in press). Therefore it is difficult to test the predictions of Dobson's (1982) and Liberg & Schantz's (1986) models. Female P. leucopus defend resources (food and their young from infanticide), and males defend females (Wolff 1985b, in press). Females have lower dispersal rates than males and they disperse shorter distances (Goundie & Vessey 1986). These results are compatible with the models of Greenwood (1980), Dobson (1982) and Liberg & Schantz (1986). However, the data parsimoniously support
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inbreeding avoidance as the ultimate causation for sex-biased dispersal. Juvenile males appear to be preprogrammed to disperse independently of density or their social environment. Adult Peromyscus tended to remain in the same home range during the breeding season, and disperse just before or just after the breeding season (Howard 1949; King 1983; Krohne & Miner 1985; Wolff 1985a). The lengths of residence for adult males and females are similar (see also Wolff 1986), but it is interesting to note the degree of dispersal of pregnant and post-lactating females. Post-weaning dispersal apparently provides living space for daughters who inherit their maternal home ranges (Wolff & Lundy 1985), but the adaptive significance of leaving an established home range just prior to giving birth is unclear. Some of the 48 females that were pregnant when they disappeared probably died, but 23 pregnant females immigrated to the grids. These immigrating females may have made preliminary exploratory movements and found suitable vacant habitat for colonizing. Peromyseus, regardless of reproductive condition, frequently switch nest sites (Howard 1949; Wolff & Hurlbutt 1982; Wolff & Durr 1986), probably to reduce the chances that a predator will locate them. Dispersal of pregnant females may be as much a response to leaving a previous home range to their first litters, as it is to finding a new nest site. We do not know whether preparturition dispersal is more common among multiparous females than primiparous females. In this study the reproductive success of immigrants was similar to that of residents, so we have no evidence for a decrease in fitness for dispersing compared to non-dispersing females.
ACKNOWLEDGMENTS We thank J. Maldonado, S. Graves and M. Maxey for their assistance in the field and with the electrophoresis. J. Cranford provided stimulating discussion on the subject, and D. Krohne, D. Fairbairn and one anonymous reviewer made helpful comments on the manuscript. This work was supported by The Theodore Roosevelt Memorial Fund, The American Museum of Natural History, the Graduate Program at Virginia Polytechnic Institute and State University, and N S F Grant 83-06619. This paper is dedicated to Frank A. Pitelka.
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(Received 30 January 1987; revised 4 May 1987; MS. number: ,~4959)