TY - JOUR
AU - Tsubota,, Toshio
AB - Abstract Natal dispersal likely plays an important role in avoiding inbreeding among large carnivores. We tested the hypothesis that male-biased dispersal reduces close inbreeding by limiting the spatial overlap of opposite-sex pairs of close relatives in brown bears (Ursus arctos) in the Shiretoko Peninsula, Hokkaido, Japan. We genotyped 837 individuals collected in 1998–2017 at 21 microsatellite loci and performed parentage analysis. To calculate natal dispersal distance, we considered the site where the mother was identified as the birthplace of her offspring, and the site where the offspring were identified as their dispersed place. As predicted, we found that dispersal distances were significantly greater for males (12.4 km ± 1.0) than for females (7.7 km ± 0.9), and those for males increased from 3 years old, indicating that males begin to disperse around the time sexual maturation begins. Relatedness decreased with distance among pairs of females, and the mean relatedness was significantly higher between pairs of females than between pairs of males or between female–male pairs within 3 km. Closely related female–male pairs rarely (5–6%) resided in close proximity (< 3 km), compared with pairs of closely related females. Our study revealed that the potential for close inbreeding was low in Hokkaido brown bears because males are effective dispersers. brown bear, dispersal, inbreeding, relatedness, Ursus arctos Natal dispersal, defined as the movement of an individual from its birthplace to the location where it will reproduce (Howard 1960), plays a major role in the demography and genetic structure of populations (Bohonak 1999; Clobert et al. 2009) and the evolution of social behavior (Waser and Jones 1983). In many species, one sex typically shows a strong tendency to disperse from their natal place, whereas the other is prone to philopatry. Four hypotheses provide potential explanations for sex-biased dispersal (Lawson Handley and Perrin 2007): inbreeding avoidance (Pusey 1987; Pusey and Wolf 1996), resource competition (Clark 1978), mate competition (Dobson 1982), and cooperative behavior among kin (Perrin and Lehmann 2001). The direction of the sex bias is determined by strategies used to compete for mates and resources. In most mammals, selection favors female-biased philopatry because females raise offspring, and daughters typically are raised in the absence of their fathers because males are polygamous (Greenwood 1980; Wolff 1993, 1994). Consequently, most males disperse to avoid inbreeding with their female kin (Costello et al. 2008). Inbreeding between closely related individuals reduces heterozygosity in populations. Inbred individuals show markedly lower survival and adaptability to changing environments than outbred conspecifics (Jiménez et al. 1994; Keller and Waller 2002). Inbreeding depression drives the evolution of strategies to avoid inbreeding, including sex-biased dispersal, specific choice of unrelated mates, kin recognition, and sperm selection (Pusey and Wolf 1996). Sex-biased dispersal builds a nonrandom pattern of relatedness among adults residing in close proximity, resulting in spatial segregation and avoidance of reproductive contact among opposite-sex relatives (Costello et al. 2008). Assessing the frequency of inbreeding and identifying inbreeding avoidance mechanisms are important for conserving species, especially small or isolated populations of large-bodied mammals (Hu et al. 2017). Brown bears (Ursus arctos) are solitary carnivores that exhibit overlapping home ranges (Dahle and Swenson 2003a) and a promiscuous mating system (Schwartz et al. 2003; Bellemain et al. 2006a). Dispersal in brown bear populations is sex-biased; males often disperse long distances and females are philopatric (Blanchard and Knight 1991; Mace and Waller 1997; Kojola et al. 2003; Shirane et al. 2018). Brown bears are widely distributed in the northern parts of the Eurasian continent and North America. In Japan, they inhabit only Hokkaido, the northernmost island (Fig. 1). The Shiretoko Peninsula, located in eastern Hokkaido, hosts one of the highest brown bear densities in the world (Hokkaido Government 2017), and contains Shiretoko National Park, a UNESCO World Natural Heritage Site. Although the Shiretoko Peninsula contains high-quality brown bear habitat, as many as 20–70 bears have been killed annually over the past decade, mainly for management purposes (Kohira et al. 2009). Past studies have reported male-biased dispersal in Hokkaido brown bears based on mitochondrial DNA subhaplotypes (Sato et al. 2011; Itoh et al. 2012; Shirane et al. 2018) and Y-chromosomal lineages (Hirata et al. 2017). The movements of individual bears should be investigated, however, to confirm this strategy in Japan. For proper conservation and management of the Shiretoko Peninsula brown bear population, it is important to understand the genetic structure of Hokkaido bears. Fig. 1. View largeDownload slide Map of the Shiretoko Peninsula, eastern Hokkaido, Japan, including the towns of Shari, Rausu, and Shibetsu. The dotted line indicates Shiretoko National Park. Fig. 1. View largeDownload slide Map of the Shiretoko Peninsula, eastern Hokkaido, Japan, including the towns of Shari, Rausu, and Shibetsu. The dotted line indicates Shiretoko National Park. The purpose of this study was to assess the potential for inbreeding among brown bears on Shiretoko Peninsula by investigating their dispersal patterns. We used a combination of field observations and molecular genetic techniques to estimate natal dispersal distances and genetic distances between all pair-wise combinations of bears. We hypothesized that male brown bears on the Shiretoko Peninsula disperse to reduce close inbreeding by spatially segregating opposite-sex, breeding-aged relatives. Using measures of genetic and geographic distance between bears that were sexually mature, our hypothesis predicted that: 1) geographic distances between male offspring and their mothers will be greater than those between female offspring and their mothers; 2) relatedness of female bears will decrease as distances among females increase, but this will not be the case for males or male-female pairs; and 3) closely related (relatedness ≥ 0.25) female-male pairs will not reside in close proximity (< 3 km) to each other. Materials and Methods Study areas and sample collection Shiretoko Peninsula (43°50′–44°20′ N, 144°45′–145°20′ E) is a long and narrow promontory (approximately 70 × 25 km) in eastern Hokkaido, Japan (Fig. 1). We collected genetic samples throughout the study area using multiple methods, dividing samples into two groups according to the collection site. The first sample set was collected in the Rusha area (44°12′ N, 145°12′ E), near the tip of the peninsula (Fig. 1). This area is designated as a special wildlife protection area where public access is not allowed without permission. There are no human residents in the Rusha area except for one fishing settlement. Additionally, because fishermen have not excluded bears from this area over the last few decades, bears have become habituated to the presence of humans, which allows researchers to observe at close range. Visual and genetic monitoring surveys have been conducted in the Rusha area since the late 1990s (Kohira et al. 2009; Shimozuru et al. 2017) and since 2008, respectively. Researchers collected genetic samples from feces, hairs collected from hair traps, and skin from biopsy darts (Shimozuru et al. 2017). The second sample set was collected in other areas throughout the peninsula, including the towns of Shari, Rausu, and Shibetsu (Fig. 1). For DNA extraction, we mostly used tissues (e.g., muscle and liver) from bears killed for nuisance control or hunting in 1998–2017. In addition, we used feces and hair collected throughout the peninsula in 2011–2017 (Shirane et al. 2018), and blood and hair samples from bears captured for research purposes in 1998–2016. We estimated the age of most bears captured or killed in 1998–2017 by counting the cementum annuli of the teeth (Yoneda 1976). All procedures involved in sample collection from live animals conformed to ASM guidelines for the use of wild mammals in research (Sikes et al. 2016), were conducted in accordance with the Guidelines for Animal Care and Use of Hokkaido University, and were approved by the Animal Care and Use Committee of the Graduate School of Veterinary Medicine, Hokkaido University (Permit Number: 1106, 1151, 1152, 15009, and 17005). Laboratory protocols We extracted genomic DNA from bear blood, muscle, and liver using a DNeasy Blood & Tissue mini Kit (Qiagen Inc., Tokyo, Japan); from hair using the DNA extractor FM Kit (Wako Pure Chemical Industries, Ltd, Osaka, Japan) or Isohair Easy (Nippon Gene Co., Ltd, Tokyo, Japan); and from feces using the QIAamp DNA Stool Mini Kit (Qiagen). We genotyped bears using 21 microsatellite markers (Ostrander et al. 1993; Paetkau et al. 1995, 1998; Taberlet et al. 1997) and one sex marker (amelogenin gene—Yamamoto et al. 2002) following protocols described in Shimozuru et al. (2017). We analyzed the allele size using an ABI PRISM 310 genetic analyzer (Life Technologies Japan Ltd.) with GeneScan ver. 4.1 software. We conducted mitochondrial DNA (mtDNA) haplotype analysis, targeting the control region (Matsuhashi et al. 1999), under conditions described in Shirane et al. (2018). We amplified a DNA fragment using PCR with TaKaRa Ex Taq polymerase (Takara Bio Inc., Shiga, Japan) and two primers (Cb-z and D4—Matsuhashi et al. 1999), and determined base sequences using the ABI Prism 310 Genetic Analyzer. We used Clustal W (ver. 2.1—Larkin et al. 2007) to identify haplotypes by comparing the nucleotide sequence of the sample with those published in a previous study (Matsuhashi et al. 1999). Parentage and relatedness We used CERVUS (ver. 3.0.7) to perform parentage analysis (Kalinowski et al. 2007). We ran CERVUS simulations for 10,000 cycles on the assumption that there were 150 candidate mothers and fathers per offspring, 40% of candidate parents were sampled, and 1% of loci were mistyped. We included a total of 837 bears as candidate offspring: 125 bears with known ages determined via field observations, 485 bears with ages estimated from their teeth, and 227 bears with unknown ages. We identified littermates (41 pairs and 5 trios) and mother–offspring relationships (49 mothers, 106 offspring, and 69 litters) by visual observations in the field and when offspring were harvested with their mothers. We included all females ≥ 5 years of age in year t (the youngest age of primiparity in this area—Shimozuru et al. 2017), present (e.g., bears killed in the year t + 1 or later), and potentially present (e.g., bears of uncertain age) in year t, as candidate mothers for a bear whose mother was unknown and estimated as being born in year t. In addition, we listed females with the same mtDNA haplotype as candidate mothers. We found seven haplotypes (HB-02, HB-10, HB-11, HB-12, HB-13, HB-New1, HB-New2—Shirane et al. 2018) and one additional heteroplasmic pattern showing an admixture between HB-10 and HB-11 (named HB-10/11). The level of admixture was variable among individuals; therefore, in the current analysis, this heteroplasmic pattern was not distinguished from HB-10 or HB-11 (i.e., both HB-10 and HB-11 females were listed as candidate mothers for individuals with HB-10/11, and vice versa). Candidate fathers included all males ≥ 3 years of age at the year t − 1, present, and potentially present in the year t − 1, based on the lowest breeding age reported in wild male brown bears (Zedrosser et al. 2007). We used two steps to assign individuals to parents using CERVUS. In the first step, we assigned a parent pair. We set the confidence level of the assignment at 80%, and allowed no mismatches in a parents-offspring combination (i.e., mother–father–offspring trio), a mother–offspring pair, or a father–offspring pair, except for mother–offspring pairs for which the relationship was confirmed by field observations. Among 106 pairs of mothers and either male or female offspring confirmed by field observations, only one pair showed one mismatched locus, which was likely a mutation. Additionally, we allowed one mismatch in a parents–offspring combination with ≥ 95% confidence level if the same mother and father were selected as likely parents (≤ 1 mismatch in a pair, ≥ 95% confidence level) in maternity and paternity assignment analyses, respectively. To avoid missing true mother–father–offspring trios, when mother–father–offspring trios showed one mismatching locus with ≥ 80% confidence level, we rechecked data from the locus causing the mismatch using single PCR to minimize the possibility of any accidental errors in the analysis. If a parent pair could not be assigned due to a low (< 80%) confidence level or the presence of ≥ 1 locus that was mismatching, we assigned maternity or paternity independently, as a second step. Even when either a mother or a father was assigned at a ≥ 80% confidence level, if the offspring had one or more candidate parents of the opposite sex that did not show any mismatches in a pair, we accepted neither parent and the parentage remained unknown. In pairs for which it was impossible to determine which member was older, for example, a pair for which the age of either or both individuals was unknown, the parent–offspring relationship remained unresolved. We calculated Lynch–Ritland relatedness coefficients (r) using the R package “related” (ver. 0.8—Lynch and Ritland 1999; Pew et al. 2014). Theoretically, the r-values for first-degree relatives (parent–offspring and full siblings) and second-degree relatives (half-siblings) are 0.5 and 0.25, respectively. Dispersal We estimated natal dispersal distance for individuals with an assigned mother and an assigned age of at least 1 year (Table 1). Offspring < 1 year of age were assumed to be dependent on their mother or unlikely to survive without their mother (Swenson et al. 2001; Shimozuru et al. 2017). Since most offspring in the Shiretoko Peninsula become independent at the age of 1 or 2 years (Shimozuru et al. 2017), we excluded yearlings and 2-year-old offspring that were accompanied by their mother based on field observations and the harvest situation. Furthermore, to reduce the potential negative distance bias associated with oversampling in the Rusha area, where philopatric offspring (i.e., dispersal distances equal zero) were sampled intensively, we excluded 13 males and 27 females born to philopatric mothers in the Rusha area and had never been observed or detected through DNA analysis outside the Rusha area (Table 1). Table 1. Number of individual brown bears (Ursus arctos) sampled in the Rusha area and other areas in the Shiretoko Peninsula, Hokkaido, Japan, 1998–2017. Category Rusha area Other areas Total Males Females Males Females Maternity assigned (age ≥ 3)a,b 17 11 54 64 146 Maternity assigned (age 1–2)a 5 0 68 30 103 Maternity assigned (age <1) 15 6 22 17 60 Maternity assigned, dependent on mother (age 1–2) 15 18 33 Maternity assigned, philopatric in the Rusha area 13 27 40 Maternity assigned, age uncertain 4 10 30 20 64 Maternity not assigned 21 24 200 146 391 Total 75 78 389 295 837 Category Rusha area Other areas Total Males Females Males Females Maternity assigned (age ≥ 3)a,b 17 11 54 64 146 Maternity assigned (age 1–2)a 5 0 68 30 103 Maternity assigned (age <1) 15 6 22 17 60 Maternity assigned, dependent on mother (age 1–2) 15 18 33 Maternity assigned, philopatric in the Rusha area 13 27 40 Maternity assigned, age uncertain 4 10 30 20 64 Maternity not assigned 21 24 200 146 391 Total 75 78 389 295 837 aIndividuals used for estimation of dispersal distances. bIndividuals included in frequency histogram of dispersal distances. View Large Table 1. Number of individual brown bears (Ursus arctos) sampled in the Rusha area and other areas in the Shiretoko Peninsula, Hokkaido, Japan, 1998–2017. Category Rusha area Other areas Total Males Females Males Females Maternity assigned (age ≥ 3)a,b 17 11 54 64 146 Maternity assigned (age 1–2)a 5 0 68 30 103 Maternity assigned (age <1) 15 6 22 17 60 Maternity assigned, dependent on mother (age 1–2) 15 18 33 Maternity assigned, philopatric in the Rusha area 13 27 40 Maternity assigned, age uncertain 4 10 30 20 64 Maternity not assigned 21 24 200 146 391 Total 75 78 389 295 837 Category Rusha area Other areas Total Males Females Males Females Maternity assigned (age ≥ 3)a,b 17 11 54 64 146 Maternity assigned (age 1–2)a 5 0 68 30 103 Maternity assigned (age <1) 15 6 22 17 60 Maternity assigned, dependent on mother (age 1–2) 15 18 33 Maternity assigned, philopatric in the Rusha area 13 27 40 Maternity assigned, age uncertain 4 10 30 20 64 Maternity not assigned 21 24 200 146 391 Total 75 78 389 295 837 aIndividuals used for estimation of dispersal distances. bIndividuals included in frequency histogram of dispersal distances. View Large We defined natal dispersal distance as the distance between the most recent location of the offspring and the most recent live location or mortality location of the mother. We used a single sampling location for individuals sampled once. When individuals were sampled multiple times, we specified locations based on the following two criteria: 1) the most recent sampling location was considered the dispersed place of the offspring; and 2) the sampling location of the mother while she was alive, even if she was later sampled as a killed bear, was considered the natal place of the offspring. We assumed that live locations were more representative of the natal range than mortality locations. We calculated dispersal distances using the “geosphere” package version 1.5–5 in R software (Hijmans 2016; R Core Team 2016). Finally, we compared dispersal distances between male and female offspring of different ages using two-way analysis of variance. We used Scheffé’s procedure (Scheffé 1953) to evaluate differences between mean values of different ages (α = 0.05). To test the prediction that geographic distances between male offspring and their mothers will be greater than those between female offspring and their mothers, we determined the frequencies of dispersal distances for offspring that were ≥ 3 years old. Three years was assumed to be the minimum age for reproductive maturity of males (White et al. 1998; Zedrosser et al. 2007), and males begin dispersal at around 3 years of age, according to our results (detailed below). We evaluated significant differences in the dispersal distances of females and males using the Wilcoxon rank-sum test. We conducted all statistical analyses using IBM SPSS Statistics for Windows ver. 20.0 (IBM Corp. 2011, Armonk, New York). Spatial-genetic relationships We restricted our analysis of spatial-genetic relationships to pairs where both individuals were alive and ≥ 3 years old during the same year because our focus was whether male-biased dispersal limits the spatial overlap of opposite-sex pairs of close relatives. We defined the year when the individual became ≥ 3 years of age as the “beginning” year, and the year when the individual died or the latest identification by field observations or genetic analysis as the “end” year. Additionally, when genetic analysis revealed that the individual was the mother or father of an offspring, we defined the latest year of known reproduction as the end year. For example, when an offspring was deceased at 2 years of age during year t, we determined the end year of its mother as year t − 2, even if she was not detected during year t − 2 or earlier. Herewith, we defined the period between the beginning and end years as the “post-dispersal period.” We assumed that pairs with overlapping post-dispersal periods lived during the same year. We examined spatial genetic structure at the individual level using geographic distances and relatedness coefficients for all pairs where both individuals in the pair were alive and ≥ 3 years old during the same year. First, we performed an isolation-by-distance (IBD) test to verify the prediction that relatedness of female bears will decrease as distance among females increases, but this will not be the case for male–male pairs or male–female pairs. Comparisons were made for female–female pairs, male–male pairs, and female–male pairs. We tested the null hypothesis of a random distribution of genotypes in space (correlation = zero) against the alternative hypothesis of a nonrandom distribution of genotypes in space (correlation = nonzero) expected under male-biased dispersal and female-biased philopatry (Peakall et al. 2003). We first computed the geographic distances between pairs based on the sampling location, and linearly regressed pairwise relatedness coefficients on the quasi-natural logarithm of pairwise geographic distances. We calculated the correlation coefficient for each comparison using R software. Then, we used a randomization method similar to the Mantel test (Mantel 1967) to account for dependence of dyadic data, as many pairs shared one individual in common. The r column was subjected to 10,000 random permutations to obtain a distribution of Mantel correlation coefficients for randomized data. We calculated the probability (P) that the absolute value of the Mantel correlation coefficient was more extreme than that of the observed value. We also used Welch’s test to compare the mean relatedness of each comparison within the same class or different classes (Welch 1938). We evaluated differences in mean r-values among each category of pairs (female–female, male–male, and female–male) using the multiple comparison test of Games and Howell (1976). Second, we determined percentage frequencies of pairs with r ≥ 0.5, 0.25 ≤ r < 0.5, 0.125 ≤ r < 0.25, and r < 0.125 for each comparison within six distance categories: 3, 6, 12, 24, 48, and 96 km. We tested the prediction that closely related female–male pairs (r ≥ 0.25) will not reside in close proximity (< 3 km) to each other by investigating whether the frequency of closely related female pairs was higher than that of closely related opposite-sex pairs within each distance category. Since annual home ranges of adult females were less than 30 km2 in the Shiretoko Peninsula (Kohira et al. 2006), we especially focused on pairs within 3 km (approximately equal to one home-range radius). In addition, we investigated the frequency within 6 and 12 km, according to the radius of minimum (115 km2 in the Oshima Peninsula; 6.1 km in radius—Institute of Environmental Sciences 2011) and maximum (462 km2 in the Shiretoko Peninsula; 12.1 km in radius—Yamanaka et al. 1995) annual home range size of adult males reported in Hokkaido. To account for differences in frequency by sex category, we used the chi-square statistic. We conducted analyses using IBM SPSS Statistics for Windows version 20.0 (IBM Corp. 2011). Results We genotyped 837 bears: 153 samples from the Rusha area in 2008–2017, and 684 from other areas on the Shiretoko Peninsula in 1998–2017 (Table 1). We genotyped all bears at all 21 loci and included them in the parentage analysis. MtDNA haplotypes were confirmed for all bears. We found seven haplotypes, HB-02 (n = 16), HB-10 (n = 122), HB-11 (n = 465), HB-12 (n = 49), HB-13 (n = 49), HB-new1 (n = 73), and HB-new2 (n = 1), and 1 heteroplasmic pattern, HB-10/11 (n = 62). Parentage analysis CERVUS assigned mothers to 446 (of 837) bears (Table 1). Among these, dependent young, individuals without age assignments, and oversampled offspring in the Rusha area were excluded. In addition to the remaining 246 individuals, we included three individuals whose mothers were confirmed though field observations. We used this sample of 249 individuals with assigned mothers and ages of ≥ 1 year old in analysis of dispersal distance. Dispersal Dispersal distance (i.e., distance between locations of the mother and offspring) differed between sexes (F1,239 = 24.263, P < 0.001) among all 249 offspring (Table 1). We detected no differences between the sexes among 1- or 2-year-old offspring, but detected differences between the sexes among 3-, 4-, and ≥ 5-year-old offspring (Fig. 2; Table 2). The dispersal distances of 3- and ≥ 5-year-old males were significantly larger than those of 1- and 2-year-old males (both P < 0.01), whereas the dispersal distances did not differ among different age classes in females (all P > 0.1). Among offspring ≥ 3 years old (Table 1), mean dispersal distance was 18.3 ± 1.4 km for males (mean ± SE, median = 16.3 km; n = 71) and 8.4 ± 1.1 km for females (median = 4.1 km; n = 75; Fig. 3). The maximum dispersal distances recorded were 59.8 km for a 3-year-old male and 47.6 km for a ≥ 5-year-old female. The Wilcoxon rank-sum test indicated a significant difference between dispersal distances of males and females ≥ 3 years old (W = 4020; P < 0.01). Table 2. Mean dispersal distances (± SE) for 249 brown bear (Ursus arctos) offspring in the Shiretoko Peninsula, Hokkaido, Japan. P-values are based on comparisons of mean dispersal distances of males versus females in each age class with Scheffé’s procedure (Scheffé 1953), following an overall two-way analysis of variance. Age (years) Dispersal distance (mean ± SE) Males versus Females Males (n) Females (n) 1 2.7 ± 0.7 km (30) 3.0 ± 0.7 km (15) P = 0.82 2 9.6 ± 1.2 km (43) 8.7 ± 2.8 km (15) P = 0.74 3 18.8 ± 2.7 km (28) 7.0 ± 1.6 km (18) P < 0.01 4 18.0 ± 2.5 km (13) 5.3 ± 1.9 km (9) P < 0.01 ≥5 17.9 ± 2.0 km (30) 9.5 ± 1.5 km (48) P < 0.01 Age (years) Dispersal distance (mean ± SE) Males versus Females Males (n) Females (n) 1 2.7 ± 0.7 km (30) 3.0 ± 0.7 km (15) P = 0.82 2 9.6 ± 1.2 km (43) 8.7 ± 2.8 km (15) P = 0.74 3 18.8 ± 2.7 km (28) 7.0 ± 1.6 km (18) P < 0.01 4 18.0 ± 2.5 km (13) 5.3 ± 1.9 km (9) P < 0.01 ≥5 17.9 ± 2.0 km (30) 9.5 ± 1.5 km (48) P < 0.01 View Large Table 2. Mean dispersal distances (± SE) for 249 brown bear (Ursus arctos) offspring in the Shiretoko Peninsula, Hokkaido, Japan. P-values are based on comparisons of mean dispersal distances of males versus females in each age class with Scheffé’s procedure (Scheffé 1953), following an overall two-way analysis of variance. Age (years) Dispersal distance (mean ± SE) Males versus Females Males (n) Females (n) 1 2.7 ± 0.7 km (30) 3.0 ± 0.7 km (15) P = 0.82 2 9.6 ± 1.2 km (43) 8.7 ± 2.8 km (15) P = 0.74 3 18.8 ± 2.7 km (28) 7.0 ± 1.6 km (18) P < 0.01 4 18.0 ± 2.5 km (13) 5.3 ± 1.9 km (9) P < 0.01 ≥5 17.9 ± 2.0 km (30) 9.5 ± 1.5 km (48) P < 0.01 Age (years) Dispersal distance (mean ± SE) Males versus Females Males (n) Females (n) 1 2.7 ± 0.7 km (30) 3.0 ± 0.7 km (15) P = 0.82 2 9.6 ± 1.2 km (43) 8.7 ± 2.8 km (15) P = 0.74 3 18.8 ± 2.7 km (28) 7.0 ± 1.6 km (18) P < 0.01 4 18.0 ± 2.5 km (13) 5.3 ± 1.9 km (9) P < 0.01 ≥5 17.9 ± 2.0 km (30) 9.5 ± 1.5 km (48) P < 0.01 View Large Fig. 2. View largeDownload slide —Mean distances (± SE) between the sampling locations of mothers and those of their male and female offspring in brown bears (Ursus arctos) in the Shiretoko Peninsula, Hokkaido, Japan. Fig. 2. View largeDownload slide —Mean distances (± SE) between the sampling locations of mothers and those of their male and female offspring in brown bears (Ursus arctos) in the Shiretoko Peninsula, Hokkaido, Japan. Fig. 3. View largeDownload slide Frequency histogram of the distances between brown bear (Ursus arctos) mothers and their offspring (≥ 3 years old): all mother–offspring pairs (n = 146), mother–daughter pairs (n = 75), and mother–son pairs (n = 71). The diamonds represent the median distance, and the lines extending from the diamonds represent the interquartile ranges. Fig. 3. View largeDownload slide Frequency histogram of the distances between brown bear (Ursus arctos) mothers and their offspring (≥ 3 years old): all mother–offspring pairs (n = 146), mother–daughter pairs (n = 75), and mother–son pairs (n = 71). The diamonds represent the median distance, and the lines extending from the diamonds represent the interquartile ranges. Spatial genetic structure and inbreeding avoidance The relatedness coefficient (r) for all pairs (n = 349,866) was −0.001 ± 0.125. The mean r of mother–offspring pairs (n = 106) confirmed by field observations (0.497 ± 0.119) was nearly identical to the theoretical r-value for parent–offspring pairs (r = 0.5), suggesting the current analysis is reliable. As predicted, the IBD test detected a nonrandom spatial genetic structure with a significantly negative correlation between the relatedness coefficient and the log-distance in female–female pairs (n = 9,991; Mantel correlation = −0.12; P < 0.001; Fig. 4). Although we detected negative correlations in male–male pairs (n = 9,348; Mantel correlation = −0.03; P = 0.002) and female–male pairs (n = 19879; Mantel correlation = −0.05; P < 0.001), the Mantel correlation value of female–female pairs was 2–4 times greater than those of male–male pairs and female–male pairs. When considering all pairs within 3 km, we found that mean r was significantly higher for female–female pairs than for male–male pairs or female–male pairs (P < 0.001). Differences in frequency by sex categories were attributed to a higher frequency of close relationships among females (Fig. 5). Within 3 km, we detected a significantly higher number of r ≥ 0.5 (2.3%) and 0.25 ≤ r < 0.5 (9.1%) relationships among female–female pairs than among either male–male pairs (0.7% and 3.9%, respectively; χ26 = 25.474, P < 0.001) or female–male pairs (0.7% and 4.6%, respectively; χ26 = 25.474, P < 0.001). Fig. 4. View largeDownload slide Mean (± SE) relatedness coefficient (r) among female-female pairs (n = 9,991), male-male pairs (n = 9,348), and female–male pairs (n = 19,879) of brown bears (Ursus arctos) ≥ 3 years old within quasi-natural logarithmic increments of distances. Fig. 4. View largeDownload slide Mean (± SE) relatedness coefficient (r) among female-female pairs (n = 9,991), male-male pairs (n = 9,348), and female–male pairs (n = 19,879) of brown bears (Ursus arctos) ≥ 3 years old within quasi-natural logarithmic increments of distances. Fig. 5. View largeDownload slide Percentage frequency of the relatedness coefficient (r) among female–female pairs (top), male–male pairs (center), and female–male pairs (bottom) of brown bears (Ursus arctos) ≥ 3 years old for different distance classes. Fig. 5. View largeDownload slide Percentage frequency of the relatedness coefficient (r) among female–female pairs (top), male–male pairs (center), and female–male pairs (bottom) of brown bears (Ursus arctos) ≥ 3 years old for different distance classes. Discussion Natal dispersal distances of brown bears in the Shiretoko Peninsula, eastern Hokkaido, Japan were 1.8–2.7 times greater for male offspring than for female offspring. These results matched our prediction that geographic distances between male offspring and their mothers will be greater than those between female offspring and their mothers, and therefore support the sex-biased dispersal hypothesis, which states that females are mostly philopatric and males are mostly dispersers (Greenwood 1980). The mean dispersal distance of males in the Shiretoko Peninsula, 18.3 km ± 1.4 (mean ± SE), was the shortest among three previously studied brown bear populations in British Columbia (23.5 km ± 1.7—McLellan and Hovey 2001), Yellowstone (77 km—Blanchard and Knight 1991), and Sweden (108.3 km ± 27.4—Støen et al. 2006). In contrast to our study, which calculated the dispersal distance using samples obtained at a certain point in time, the studies described above used radiocollars and tracked the bears over extended periods. Since the latter method could restrict analysis to individuals who have completed dispersal, this methodological difference might have led to the shorter distances found in this study. In addition, one factor leading to this difference may be the variation in the home range size among these bear populations. Shorter dispersal distances likely reflect smaller home ranges in bears (McLellan and Hovey 2001). The home range size for adult males in the Shiretoko Peninsula is not well known, but was preliminarily reported as 199–462 km2 (n = 2) in the Shiretoko Peninsula (Yamanaka et al. 1995; Kohira et al. 2006), and approximately 297 km2 (in 10 months) and 115 km2 (in 2 months) in the Oshima Peninsula, southwestern Hokkaido (Institute of Environmental Sciences, Hokkaido Research Organization 2011). These sizes are smaller than the 668 ± 331, 874, and 833–1,055 km2 sizes estimated in British Columbia (McLellan and Hovey 2001), Yellowstone (Blanchard and Knight 1991), and Sweden (Dahle and Swenson 2003b), respectively (all of them were estimated by Minimum Convex Polygons). The estimated dispersal distances in British Columbia, Yellowstone, Sweden, and the Shiretoko Peninsula suggest that bears disperse at least 0.80–3.28 times farther than their home range diameter. Dispersal distances also may be affected by population density. Negative relationships between population density and home range size, and between density and dispersal distances, have been reported in bears (Oli et al. 2002; Dahle and Swenson 2003b; Støen et al. 2006; Roy et al. 2012). Brown bear density in the Shiretoko Peninsula was estimated as 318–324 bears/1,000 km2 (Hokkaido Government 2017), which is much greater than the average density of 80 bears/1,000 km2, 12 bears/1,000 km2, and 11–29 bears/1,000 km2 observed in British Columbia (McLellan 1989), Yellowstone (Haroldson et al. 2013), and Sweden (Støen et al. 2006), respectively. In a high-density area, due to short distances between unrelated individuals, even a short dispersal from the natal place can successfully decrease the relatedness of pairs residing in close proximity, resulting in inbreeding avoidance (Cockburn 1985). We hypothesize that brown bears disperse short distances because they have small home ranges and ample resources on the narrow Shiretoko Peninsula. There are several rivers in the Shiretoko Peninsula where large numbers of spawning pink salmon migrate in autumn (Nakamura and Komiyama 2010); such a rich food source may be responsible for their relatively high density, small average home ranges, and short dispersal distances. Two sampling methods may have biased our results in favor of shorter dispersal distances. First, we only collected samples inside the Shiretoko Peninsula, which provides no information about dispersal between the peninsula and mainland Hokkaido. The length of the central axis of the peninsula precluded detecting dispersers that traveled more than 70 km. The frequency histogram of dispersal distances showed that the median distance of males aged ≥ 3 years was ~ 16 km and few males dispersed more than 40 km (Fig. 3). These results suggest that there are few, if any, long-distance dispersers in this population. Second, as most of the samples analyzed in this study were obtained from dead bears via nuisance control or hunting, some bears may have been killed while dispersing. Throughout the lower part of the peninsula, there are vast agricultural farms that produce mainly dent corn and sugar beets. These farms may act as an “attractive sink” because of the availability of human-derived foods, which led to human-caused bear mortalities (Delibes et al. 2001; Sato et al. 2011). Shirane et al. (2018) documented that males with the HB-02b mitochondrial DNA subhaplotype, which was distributed in central Hokkaido outside of the peninsula, have dispersed to the lower part of the peninsula. These males, however, were detected only in the lower peninsula, indicating that dispersal by males may be restricted in the lower peninsula because of nuisance control or hunting (Matsuhashi et al. 1999). Anthropogenic deaths in the attractive sink may bias brown bears toward shorter dispersal distances in the Shiretoko Peninsula. As predicted, mean relatedness of female bears decreased as distance among females increased, although relatedness between male–male pairs and female–male pairs also declined. Additionally, in female–female pairs, the proportion of relatives living in close proximity was larger than expected if random, whereas males were located at random compared with their relatives. These results are consistent with male-biased dispersal and female-biased philopatry (Roy et al. 2012). A similar spatial genetic structure has been documented for brown bear populations in Scandinavia and a black bear (Ursus americanus) population in New Mexico (Støen et al. 2005; Costello et al. 2008), where dispersal was also male-biased. The significant increase in dispersal distance in male bears suggests that males start to disperse at age 3 years in the Shiretoko Peninsula. Males are often found outside their mother’s home range at 2 or 3 years old in British Columbia (McLellan and Hovey 2001), and in Sweden, one-half of the males start to disperse at 2 years old, and 81–92% of males have dispersed before reaching 5 years of age (Støen et al. 2006). Dispersal by males at 2–5 years in the Shiretoko Peninsula, British Columbia, and Sweden may be related to the age of sexual maturation. The youngest breeding age previously reported is 3 years for males in Sweden, whereas in Montana and Wyoming, sexual maturity is attained by males at approximately 5.5 years old (White et al. 1998; Zedrosser et al. 2007). These results were consistent with our prediction that males effectively disperse from their natal area around the age of acquiring sexual maturation, which possibly affects inbreeding avoidance. Although the dispersal distances for males were shorter than those in other populations, the potential for close inbreeding remained low. We estimated that 83–94% of the opposite-sex pairs sampled within 3 km were unrelated, suggesting that closely related female–male pairs rarely reside in close proximity to each other. Only 1% and 5% of female–male pairs appeared to involve parent–offspring or full-sibling relationships (r ≥ 0.5) and half-sibling relationships (0.25 ≤ r < 0.5), respectively. Thus, bears in the Shiretoko Peninsula have a risk of inbreeding of only 5–6%, indicating that dispersal distances of ≥ 3-year-old males were effective in reducing overlap with close relatives. In addition, ~ 35% of closely related (r ≥ 0.25), opposite-sex pairs (17 of 49) within 3 km included males less than 6 years old. Since young and small individuals rarely participate in breeding (Craighead et al. 1995), the actual risk of inbreeding was likely to be lower than the risk estimated from the overall frequency of proximity of relatives. The potential risk of inbreeding between parents and offspring was similar (2.1%) to father–daughter mating in a Scandinavian brown bear population (Bellemain et al. 2006b). Among relatives of opposite-sex pairs residing near each other, father–daughter relationships are expected to be the most probable, given female-biased philopatry (Costello et al. 2008). In this study, we found no trend toward increased dispersal distances as males became older. Costello (2008) also documented that male bears did not abandon their established home ranges after the age of 6 years. These findings suggest that a male that remained in one area for a long period may mate with his mature daughter. In the Shiretoko Peninsula, however, harvesting via nuisance control and hunting can promote turnover of mature males, which may result in a decreased probability of inbreeding. In conclusion, we revealed male-biased dispersal and its influence on spatial genetic structure in the brown bear population of the Shiretoko Peninsula, eastern Hokkaido, Japan. Despite the shorter dispersal distances of Hokkaido brown bears compared to those of bears in British Columbia, Yellowstone, and Sweden, the potential for close inbreeding remains low, indicating that male-biased dispersal effectively prevents inbreeding. We hope that these findings will contribute to the conservation and management of brown bear in Japan and other populations worldwide. Acknowledgments We thank H. Ose and all the members of the Shiretoko Fishery Productive Association for their generous support. We are grateful to all the members of the Shiretoko Nature Foundation and South Shiretoko Brown Bear Information Center for their generous support. We thank J. Moriwaki, S. Hirano, N. Nagano, F. Mori, and M. Tsujino for contribution to sample collection and field research. 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Google Scholar Crossref Search ADS PubMed WorldCat Author notes Both authors contributed equally to this work © 2019 American Society of Mammalogists, www.mammalogy.org This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Sex-biased dispersal and inbreeding avoidance in Hokkaido brown bears
JO - Journal of Mammalogy
DO - 10.1093/jmammal/gyz097
DA - 2019-07-27
UR - https://www.deepdyve.com/lp/oxford-university-press/sex-biased-dispersal-and-inbreeding-avoidance-in-hokkaido-brown-bears-wXFJVC0eCD
SP - 1317
VL - 100
IS - 4
DP - DeepDyve
ER -