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Paternity success for resident and non-resident males and their influences on paternal sibling cohorts in Japanese macaques (Macaca fuscata) on Shodoshima Island
Paternity for male Japanese macaques on Shodoshima Island
https://orcid.org/0000-0003-2194-0387
Ishizuka Shintaro Conceptualization Data curation Formal analysis Funding acquisition Investigation Methodology Project administration Writing – original draft Writing – review & editing 1 2 3 4 *
Inoue Eiji Resources Supervision 2
Kaji Yuki Data curation Investigation 5
1 Faculty of Life Science and Technology, Department of Biological Science, Fukuyama University, Fukuyama, Hiroshima, Japan
2 Faculty of Science, Department of Biology, Toho University, Funabashi, Chiba, Japan
3 Japan Society for Promotion of Science, Kojimachi Business Center Building, Chiyoda-ku, Tokyo, Japan
4 Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
5 Choshikei Monkey Park, Tonosho, Kagawa, Japan
Santacà Maria Editor
University of Vienna: Universitat Wien, AUSTRIA
Competing Interests: The authors have declared that no competing interests exist.

* E-mail: ishizuka.shintaro@fukuyama-u.ac.jp
19 9 2024
2024
19 9 e03090561 7 2024
6 8 2024
© 2024 Ishizuka et al
2024
Ishizuka et al
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Reproductive success can be attributed to both resident and non-resident males in non-human primates. However, reproductive success of non-resident males has rarely been investigated at an individual level. As resident males achieve different degree of reproductive success with regard to various factors, such as male dominance relationships or female mate choice, the degree of reproductive success for non-resident males may vary between individuals. As male reproductive success is highly skewed towards specific individuals, the percentage of similar-aged paternal siblings within groups is expected to increase. However, the extent to which each male contributes to the production of cohorts of paternal siblings remains unclear. Here we examined the paternity of offspring born over five consecutive years in a free-ranging group of Japanese macaques Macaca fuscata on Shodoshima Island, Kagawa Prefecture. Genotypes of 87 individuals at 16 autosomal microsatellite loci were analyzed and paternity of 34 offspring was successfully assigned to a single candidate father. We quantitatively assessed paternity success for resident and a few non-resident males whose genetic samples were successfully collected. We quantitatively assessed the percentages of paternal siblings in the same age cohorts produced by those males. Non-resident males sired similar percentage of offspring compared to resident males. A large prime-aged non-resident male was the most successful sire among males in two of the five years. These results provide new insights that male reproductive success could be highly skewed toward a specific non-resident male. Subadult males had a lower percentage of paternity success, which may be because females may prefer physically mature males. Various males, including non-resident males, contributed to the creation of paternal sibling in the same age cohort. The overall results highlighted that not only resident but also non-resident males play an important role in shaping within-group kin structures.

http://dx.doi.org/10.13039/501100001691 Japan Society for the Promotion of Science 22K15191 https://orcid.org/0000-0003-2194-0387
Ishizuka Shintaro http://dx.doi.org/10.13039/501100001691 Japan Society for the Promotion of Science 21J00922 https://orcid.org/0000-0003-2194-0387
Ishizuka Shintaro Cooperative Research Program of the Wildlife Research Center, Kyoto University 2020-B-05 https://orcid.org/0000-0003-2194-0387
Ishizuka Shintaro Leading Graduate Program in Primatology and Wildlife Science, Kyoto University https://orcid.org/0000-0003-2194-0387
Ishizuka Shintaro This study was financially supported by the JSPS KAKENHI (21J00922 and 22K15191 to SI), Cooperative Research Program of the Wildlife Research Center, Kyoto University (2020-B-05 to SI), and Leading Graduate Program in Primatology and Wildlife Science, Kyoto University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Data AvailabilityAll relevant data are within the paper and its Supporting Information files.
Data Availability

All relevant data are within the paper and its Supporting Information files.
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pmcIntroduction

Male competition over access to females plays important roles to secure breeding opportunities in animals [1,2]. As a consequence of male–male competition, males often achieve different degrees of reproductive success. In group-living primates, variance in reproductive success among males is sometimes explained by dominance relationships [3–6]. Studies have shown that reproductive success is often skewed toward high-ranking males within multimale groups [7–13]. Beside dominance relationships, female mate choice also can affect the distribution of male reproductive success [14,15]. Females may prefer to mate with particular categories of males, depending on the characteristics of males, such as their maturity, capacity for investment, or genetic background [16,17]. Males that are selected by females can achieve high reproductive success [18–22].

Variance in male reproductive success has been investigated within social groups. Yet, reproductive success for males outside a group has been infrequently examined. In group-living animals, especially primates, both resident and non-resident males have opportunities to breed with females of the group. The paternity of offspring assigned to males outside a group is termed extra-group paternity (EGP). EGP is a phenomenon widely observed in various primate species [23–28] and is essential for the evolution of social systems in animals as it increases genetic diversity within groups and is consequently associated with the increased chance of offspring survivorship [29]. EGP has been usually determined when the paternity of offspring is unsuccessfully assigned to all candidate fathers within a group, probably because individual identification and sample collection for non-resident males are usually difficult in the field. Several studies that have examined the overall percentages of EGP have shown that their percentages would increase when the number of males within groups decreases or when female reproductive synchrony increases [26,30,31]. However, few studies have assigned EGP to a particular non-resident male, and the number of cases in which paternity success for each non-resident male has been assessed at the individual level is scarce [32]. Similar to the pattern in resident males, the degree of reproductive success for each non-resident male may vary depending on various factors, such as their dominance relationships or female choice. To understand mechanisms that influence the variance in the male reproductive success among all types of males, it is necessary to assess the reproductive success for not only the resident males, but also the non-resident males, by individually identifying and sampling both.

Variance in the male reproductive success modulates the abundance of paternal kin living in animal groups. The presence of kin within groups plays important roles for their social lives because kinship is one of the key factors that affects affinity among individuals, and reciprocity and cooperation are attributed to kin selection [33–35]. There is evidence of paternal kin bias behavior in primates [36–39]. The evidence suggests that primate individuals have more social partners as the number of paternal kin increases in their groups. Theoretically, the percentage of paternal sibling dyads in the same age cohort is expected to increase with a higher male reproductive skew [40–42]. Since male reproductive success is often skewed toward the highest-ranking males in primate groups, researchers have assessed the percentage of paternal sibling dyads in the same age cohort according to the percentage of paternity success by the highest-ranking male [38,42,43]. However, the paternity success can be skewed towards other resident males or non-resident males besides the highest-ranking male. The contributions of those non-highest-ranking males to the percentages of paternal sibling dyads in the same age cohorts have not been investigated. For a comprehensive understanding of the mechanisms that produce kin-dyads within animal groups, it is crucial to examine the percentages of paternal sibling dyads produced by non-resident males at an individual level.

The Japanese macaque (Macaca fuscata) provides an interesting opportunity for the investigation of paternity success of non-resident males and their contributions to the production of within-group kin-dyads. They form female-philopatric multi-male and multi-female groups characterized by strong matrilineal affiliative relationships and a polygynandrous mating system [44–51]. Males typically emigrate from their natal group when they are approximately four or five years old [52] and continue to transfer between groups throughout life [53]. The tenure of males in a group is approximately three years [54]. Dominance rank is linear and stable in both sexes [54–56], although troop takeovers by non-troop males were reported from the Yakushima population [57]. Non-resident males often breed with females of the group, as the percentages of EGP are relatively high among primates [28,31]. This is partially because they have breeding seasonality [58,59], and novel and unfamiliar males attain high reproductive success because they are strongly selected by females for mating partners when females are likely to conceive [19,21,60,61]. Further, the exact number of siring for each non-resident male in the field can also be assessed. During the mating season, several non-resident males sporadically appear around the group and copulate with the group’s females [24,62]. Considering that previous field research succeeded in collecting behavioral data and genetic samples from non-resident males [19,24,63], it is possible to expand on it further to examine the paternity success for non-resident males at the individual level. Moreover, the percentage of paternity by the highest-ranking male is usually low [19,24,64], although one study reported a relatively high percentage [65]. This suggests that the percentages of paternal sibling dyads produced by non-resident males can be assessed quantitatively.

In this study, we examined the paternity of the offspring born in five consecutive years within a group of Japanese macaques, wherein resident and a few of non-resident males were identified and sampled. We assessed the percentages of paternity success for both resident and non-resident males and the percentages of paternal sibling dyads produced by them among the offspring in each year.

Materials and methods

Study subjects

The study subjects were free-ranging Japanese macaques of the B-group inhabiting an area near the Choshikei Monkey Park on Shodoshima Island [51]. The macaques are provisioned by park staff at approximately 8:30 h, 14:00 h, and 16:00 h and by tourists visiting the park. We initially conducted field research on the subjects and started individual identification of the group between September and December 2017. In April 2018, we started monitoring the presence of identified individuals in the monkey park on a daily basis (five or six days per week), although their presence has not been systematically recorded. In February 2019, we successfully completed individual identification of group members, and started systematically recording the daily presence of the members of the group. The mean number of observation days per month for 2019–2022 was 25.6. The group size, the number of adult females, and the number of adult and subadult males for 2019–2021 are shown in Table 1.

10.1371/journal.pone.0309056.t001 Table 1 Composition of the B-group at the end of 2019–2021.

	2019	2020	2021	
Adult females	29	16	16	
Adult and subadult males	12	13	11	
Juveniles and infants	40	35	33	
Group size	81	64	60	
The number of group members gradually decreased from 2019 to 2020. Although the reason for the decline remains unclear, this might be because several members were captured by the government or local people.

Classification of males

This study focused on males estimated to be aged ≧ 4 years and sexually mature [66]. They were classified based on their age class and social status. Following a previous study [19], the age class of males aged 4–6 years and that > 6 years was categorized as “subadult” and “adult,” respectively.

For this study, the males were first divided into resident males of the study group or non-resident males according to the daily monitoring. After completing individual identification of the study group in February 2019, we sometimes encountered unidentified males around the mating season. Those males were seemingly unhabituated to human observers and did not eat provisioned food, implying that they were not members of the group. We regarded those males as “non-resident males”. We identified four non-resident males during the study period.

The social status of the resident males was further divided into dominant or subordinate males. Males of provisioned groups constantly compete with one another over food, which emphasizes the dominance-subordinate aspects of their relationships [67]. In our study, some males were allowed to access preferred food at the provisioning area, whereas other males were driven away by both the males and females who stayed at the provisioning area and were thus uncommonly observed to enter into the area. Therefore, we classified those males that were allowed to access the provisioning area as dominant and those that were driven away from the provisioning area as subordinate males. Collectively, the social status of males was classified into three categories: dominant, subordinate, and non-resident males. This is in accordance with previous studies on macaque species [24,68]. Two to three dominant, eight to ten subordinate, and two identified non-resident males were present between 2019 and 2021, respectively. The presence and social/age class of all identified males in each mating/non-mating season is shown in S1 Table. We regarded September–December as the mating season, and January–August as the non-mating season because births occur between March and June [58,59], and the mean gestation length of this species is 176 days [69].

Genetic analysis

We used genotype data for the study subjects at 16 autosomal microsatellite loci, which were obtained in our previous work [51]. The study estimated dyadic genetic relatedness between females within the study group to assess the strength of kin relationships between them. Since this study newly assessed paternity success for resident and non-resident males, this study does not constitute dual publication. Feces, sperm, and saliva samples were collected using cotton swabs and stored in lysis buffer at ambient temperature immediately after we observed defecation, ejaculation, and materials the animals sucked in the field. DNA was extracted from the samples using a QIAamp Stool Mini Fast Kit (Qiagen, CA, USA). Using DNA extracts, the genotypes at 16 autosomal microsatellite loci were analyzed using the multiplex PCR method [70]. Amplification products were separated by capillary electrophoresis using an ABI 3130xl Genetic Analyzer (Applied Biosystems, CA, USA). Alleles were sized using Peak Scanner (Applied Biosystems). Since DNA extracted from non-invasively collected samples is typically degraded and low in concentration [71,72], we repeated the genotyping to ensure accuracy following the criteria in the previous study [70]. Details for the methods of genetic analysis are described in a previous study [51].

Paternity analysis

The paternity of 46 offspring (8 of 18 in 2018, 9 of 19 in 2019, 8 of 13 in 2020, 10 of 10 in 2021, and 11 of 11 in 2022, respectively) was investigated. The offspring whose paternity was not investigated were already missing and no genetic samples had been collected from them. Paternity analysis was conducted using the pairwise likelihood approach with CERVUS [73]. The resident candidate fathers were only fully sampled for the offspring born in 2020, 2021, and 2022. Therefore, the percentage of EGP could be calculated for only these years. According to our field observations, there seemed to be approximately 10 unsampled candidate fathers who belonged to the group during the 2017 and/or 2018 mating seasons or were non-resident males. Since we collected genetic samples for 19 candidate fathers, which included three of the four identified non-resident males and accounted for 60–70% of all candidate fathers, the proportion of sampled candidate fathers was eventually assumed to be 0.60. The proportion of loci mistyped and the error rate in the likelihood calculation was both 0.01 because genotype accuracy was confirmed following reasonable criteria [70]. Paternity for 42 of the 46 offspring was analyzed under the condition that the offspring’s maternity was known since genotypes for the mothers were determined. However, genetic samples for mothers of four offspring could not be collected. Therefore, the paternity for the four offspring was analyzed under the condition that the maternity of the offspring was unknown. When the most likely father had no mismatched alleles and the confidence level for the assignments was more than 95%, the male was concluded to be the offspring’s father.

Statistical analysis

To analyze the likelihood of siring by each male, we constructed generalized linear mixed models (GLMMs) with binomial distribution and logit link function. We included the percentage of sires for each male in each year as a response variable. Since the total number of sampled males was 10, 10, 12, 12, and 13 in 2017, 2018, 2019, 2020, and 2021, respectively, the total number of data points was 57. The response variable ranged from 0 to 0.40, as the most successful sire’s share in a year was 40% (see the Results). The social status (dominant/subordinate/non-resident) and age class (adult/subadult) of each male and the number of newborns, which corresponds to the approximate number of estrus capable females in each year (18 in 2018, 19 in 2019, 13 in 2020, 10 in 2021, and 11 in 2022), were included as predictor variables. Offspring ID and the study year were included as random effects. We calculated the Akaike’s information criterion (AIC) for the constructed model and null model. Comparing the AIC values, we assessed the fit of constructed model. The models were fit using the “lmer” function of the R package lme4 [74].

Ethics statement

This study was permitted by the Choshikei Monkey Park on Shodoshima Island, Japan. All methods were designed to be noninvasive for the subjects. Field research was conducted in accordance with the American Society of Primatologists Code of Best Practices for Field Primatology, and conformed to the Guidelines for Field Research established by the Ethics Committee of the Primate Research Institute of Kyoto University. All aspects of this study adhered to the ASAB/ABS Guidelines for the use of animals in research.

Results

Paternity

Genotypes of the 88 individuals at 16 autosomal microsatellite loci were analyzed (S2 Table). The number of alleles, heterozygosity, and allelic dropout rate are investigated based on the genotypes (S3 Table). The paternity of 34 of the 46 offspring was assigned to a single candidate father (Fig 1 and S4 Table). At least one offspring was sired by sampled non-resident males in each year. Since all resident candidate fathers for offspring born in 2018 and 2019 were not sampled, it remains unclear whether or not these offspring were sired by non-resident males, and thus, the percentage of EGP could not be calculated for those years. However, for the years in which all resident candidate fathers were sampled, the results revealed that the percentage of EGP was 50% (4 of 8) in 2020, 50% (5 of 10) in 2021, and 9% (1 of 11) in 2022. The overall percentage of EGP between 2020 and 2022 was 34% (10 of 29). Interestingly, 75% (3 of 4) and 80% (4 of 5) of the EGP cases were assigned to a single non-resident male “NP” in 2020 and 2021, respectively. He was the most successful sire and sired 38% (3 of 8) and 40% (4 of 10) of offspring in 2020 and 2021, respectively. The proportion of paternity success for each male across the study years is shown in S5 Table.

10.1371/journal.pone.0309056.g001 Fig 1 The number of offspring sired by each male in the five-year study period.

Gray, lined, and dot bars indicate sires by the dominant, subordinate, and non-resident males, respectively. White bars indicate sires whose father’s social status remained unclear. The ID of all fathers is shown in each bar. The values within brackets represent the number of paternities analyzed in each year.

Effects of male categories on the percentages of paternity success

The constructed model was significantly better fit than the null model (ΔAIC = 10.99, P < 0.001). The constructed model showed that the effects of neither male social status nor the number of estrus capable females were significant (Fig 2A and Table 2). The effect of male age class had a negative effect on the percentage of paternity success, indicating that paternity success of subadult males was lower than that of the adult males (Fig 2B and Table 2).

10.1371/journal.pone.0309056.g002 Fig 2 The effects of males’ social status and their age class on their paternity success.

Proportion of paternity success by each male in each year according to the males’ social status (A) and their age classes (B) are shown. Boxes indicate the first to third quartile of observed values, solid lines show the median, and each dot represents the proportion of paternity success by a sampled candidate father in each year.

10.1371/journal.pone.0309056.t002 Table 2 Results of the generalized linear mixed model (GLMM) performed to test the effects of males’ social status and their age class.

Parameter	Log-Odds	SE	95% CI	Z	P	
(Intercept)	−1.60	1.10	−3.76 to 0.55	−1.46	0.145	
Male category (non-resident vs. dominant)	0.47	1.09	−1.67 to 2.60	0.43	0.669	
Male category (non-resident vs. subordinate)	0.11	0.75	−1.37 to 1.58	0.14	0.888	
Age (adult vs. subadult)	−3.00	1.05	−5.06 to −0.95	−2.86	< 0.01	
No. of capable females	−0.08	0.06	−0.21 to 0.04	−1.26	0.208	

The proportion of paternal sibling dyads

The percentages of paternal sibling dyads among the offspring born in 2018, 2019, 2020, 2021, and 2022 were 0%, 8%, 14%, 27%, and 16%, respectively (Table 3). The overall percentage of paternal sibling dyads was 15%. Interestingly, subordinate males or non-resident males produced 11–13% of paternal sibling dyads between 2020 and 2022.

10.1371/journal.pone.0309056.t003 Table 3 The percentage of paternal sibling dyads among offspring born in each year. The values within the brackets represent the number of paternal sibling dyads in each category.

Year	No. of dyads analyzed	Percentage of paternal sibling dyads	Maximum percentage of paternal sibling dyads produced by one male	Male category of the most successful sire	
2018	28	0(0)*	N/A	N/A	
2019	36	8(3)*	N/A	N/A	
2020	28	14(4)	11(3)	NR	
2021	45	27(12)	13(6)	S and NR	
2022	55	16(9)	11(6)	S	
Total	192	15(28)	12(15)	-	
S and NR represent subordinate and non-resident males, respectively. N/A represents data that was not available.

* The percentages may have been underestimated because offspring whose fathers remain unidentified may have been paternal siblings.

Discussion

The percentage of EGP between 2020 and 2022 was 34% (9–50%) in the Shodoshima B-group. These results are consistent with previous results showing that 23–80% of offspring were sired by non-resident males (Table 4). The percentage of EGP in this species is relatively high among primate species [28,31]. One reason for the relatively high percentage of EGP may be the high extent of female receptive synchrony in this species [65]. EGP is more likely when the number of males within groups decreases and when female reproductive synchrony increases [26,30,31]. Similar to other species that exhibit both high female receptive synchrony and EGP, resident males may not guard receptive females against non-resident males.

10.1371/journal.pone.0309056.t004 Table 4 Overview paternity results in Japanese macaques.

Site	Number of adult males	Number of adult females	Condition of study site	Period	Number of paternity	Maximum percentage of paternity for one male (%)	Note for the status of the most successful sire	Overall EGP (%)	Reference	
Kyoto University	19	30	Captive	1988	48	22.9	Highest-ranking	-	[64]	
Yakushima, Nina-A	15	15	Wild	1998	9	22.2b	Highest-ranking	33	[65]	
Yakushima, Nina-A	7–10	2–7	Wild	1999–2000	4	25	Low-ranking, and non-resident	25	[24]	
Yakushim, B	1–7	6–7	Wild	1996–2000	5	20b	High-ranking, low-ranking, and non-resident	80	
Arashiyama	24–27	93–100	Free-ranging	2002–2003	23	15.3	Low-ranking	23	[19]	
Oregon	17	N/A	Semi free-ranging	2018–2019	34	20.5	High-rankingc	-	[21]	
Shodoshimaa	11–13	16–29	Free-ranging	2019–2021	46	27.5	Non-resident	34	Present study	
a The data in 2018 and 2019 were excluded because of incomplete individual identification.

b The percentage may become higher if EGP is attributed to the single male.

c It remains unclear whether the male was the highest-ranking male.

A non-resident male, “NP,” was the most successful sire in both 2020 and 2021. Our results highlighted that at least some proportion of non-resident males could have chances to gain a high percentage of paternity success, although the reproductive success of non-resident males as a whole cannot be assessed because of the incomplete sampling of non-resident males. Given that the non-resident males sampled in this study might have chances to breed with females of other groups beside our study group, the percentage of paternity success for these non-resident males might have been underestimated. Since female Japanese macaques prefer to mate with unfamiliar males [75,76], non-resident males may maintain unfamiliarity with females for at least several years, and consequently have several chances to breed with females. Furthermore, our results provide new insights that there is a reproductive skew among non-resident males; 75–80% of EGP were attained by “NP” in 2020 and 2021, while “TN” was unsuccessful in siring offspring in those two years. According to our field observations, “NP” was a large prime-aged male and displayed frequently (Fig 3). A previous study in captivity showed that female Japanese macaques expressed mate choice behavior toward males who displayed most frequently when they were likely to conceive [61]. Since non-resident males are typically unfamiliar to females and the extent of unfamiliarity to females might not differ between them, a non-resident male who displayed frequently might be favored as females’ mating partner and gain higher paternity success.

10.1371/journal.pone.0309056.g003 Fig 3 A photograph of the non-resident male who attained a high percentage of paternity success.

His individual ID was “NP”.

Notably, subadult males sired a lower percentage of offspring than the adult males. These results were consistent with previous studies showing that males reach high reproductive success when they are approximately six years old in rhesus macaques Macaca mulatta [77,78], and subadult males (aged 4.5–6.5 years old) had a much lower reproductive success than adult males (7.5–25 years old) in Barbary macaques Macaca sylvanus [79]. The tendency in which males who reach an age of approximately six years old can gain high amounts of reproductive success may be common among macaque species, although all of these results were observed in provisioned or semi-closed environments. Age-related variance in male reproductive success may be influenced by a function of the interaction between social skills and morphological traits [80,81], or facial coloration of males [82–84].

The percentage of paternal sibling dyads among offspring in the same age cohort was 15% (8–27%) in the Shodoshima-B group. Although available data for comparisons with our results is scarce, the percentage is relatively high compared to 12% in rhesus macaques [42] and 5% in Assamese macaques Macaca assamensis [38]. As shown in Table 4, the most successful sires were the highest-ranking males in only two or three of the seven cases. These results suggest that various males, including non-resident males, contribute significantly to the production of paternal sibling dyads in Japanese macaques. The presence of paternal sibling dyads in the same age cohort may trigger kin selection and enhance affinity among individuals of same age. In female-philopatric primates, females of same or similar age often form strong affiliative relationships (e.g. brown capuchin monkeys Cebus apella nigritus: [85]; chacma baboons Papio hamadryas ursinus: [86]; rhesus macaques: [87]). In Japanese macaques on the Katsuyama population, the two subject females of the same age formed long-term grooming partnerships [49]. Such an affinity among same or similar-aged individuals in Japanese macaques may be favored by paternal sibling relationships, although it is unclear whether individuals can discriminate paternal kin. Future behavioral and genetic studies are required to clarify the presence or absence of paternal kin bias in this species.

Our findings contribute to a better understanding of how male social status influences diverse reproductive strategies. Notably, this study clearly showed that at least some non-resident males can attain high reproductive success. Furthermore, various males, including non-resident males, significantly contribute to the production of paternal sibling dyads in the same age cohorts, suggesting that not only the resident males, but also non-resident males play an important role in shaping within-group kin structures. However, future studies are required to examine how paternal siblings interact with each other.

Supporting information

S1 Table Information for candidate fathers.

(DOCX)

S2 Table Genotype data for 88 individuals of the B group.

(XLSX)

S3 Table Summary for population genetic parameters.

(DOCX)

S4 Table Results for paternity of offspring in the B group.

(DOCX)

S5 Table Proportion of paternities for each male across the study years.

(XLSX)

We thank Dr. K. Watanabe, Mr. A. Nishio, Ms. C. Saeki, Mr. M. Ishii, Ms. K. Miyashita, and Mr. K. Hida for their help with the fieldwork. English language editing was provided by Editage (https://www.editage.jp).

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PONE-D-24-26360Paternity success for resident and non-resident males and their influences on paternal sibling cohorts in Japanese macaques on Shodoshima IslandPLOS ONE

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Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #2: Yes

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Reviewer #2: No

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Reviewer #1: I was enthusiastic in my reading of the original manuscript, and my enthusiasm has only grown with these careful and substantial revisions. I would like to sincerely thank the authors. There is nothing more frustrating than peer-reviewing a manuscript only to have your comments ignored. I appreciate the respect and thoroughness with which the authors addressed my comments and suggestions. I look forward to seeing this paper published with the full fanfare and acknowledgement it deserves. My remaining (minor) comments are below:

1. I would include the scientific name in the title of your article

2. I would combine the first two sentences of your introduction to read something like "Male competition over access to females is central to securing breeding opportunities in many species".

3. I would replace the word "animal" with "social" at L65

4. The paragraph from L65-L85 is great!! Really concise but clear explanation of the knowledge gap your study is filling.

5. I would revise the sentence at L89-90 to read "There is evidence of paternal kin-biased behavior in primates" for clarity.

6. I would revise the sentence starting at L102 to read something like "Japanese macaques (Macaca fuscata) provide an interesting opportunity for the investigation of paternity success of non-resident males and their contributions to the production of within-group kin-dyads"

7. L104 Is "bisexual" really the word you're looking for? If you're referring to multiple males and females mating with each other, you might be looking for the word "polygynandrous".

8. I would generally rephrase L104 to read "They form female-philopatric multi-male and multi-female groups characterized by strong matrilineal affiliative relationships and a polygynandrous mating system"

9. L110 "Noteworthily" reads a bit odd to me. I would remove.

10. Has a high percentage of EGPs been previously recorded for Japanese macaques specifically? Or is L110-111 referring to other species?

11. Thank you for expanding table 1 :)

12. Methods overall are greatly improved and offer better detail and clarity!

13. I have no comment on genetic methods as this is not my area of expertise.

14. Very interesting results. The discussion appropriately contextualizes the results within the limitations of the study. I appreciate the comparisons to other specific studies and species.

Great work, authors!

Reviewer #2: Thank you for the opportunity to review this interesting manuscript. The authors set out to examine the reproductive success of non-resident:resident male Japanese macaques in a provisioned, habituated population. There is little information on non-residents in the published literature, so this represents a unique and important contribution to the literature. Additionally, the authors calculated the number of paternal siblings in the study group, which will aid in our understanding of how kinship influences social behavior. The authors have revised the manuscript and addressed the previous two reviewers' concerns in my judgement. I recommend publication following minor revision. I used track changes in the attached document to help the authors find places where I changed sentences or had questions regarding their meaning. I wish them the best of luck with future work at this site.

**********

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Reviewer #2: No

**********

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Attachment Submitted filename: PONE-D-24-26360_reviewer.docx

10.1371/journal.pone.0309056.r003
Author response to Decision Letter 0
Submission Version1
1 Aug 2024

Academic Editor: I have carefully read the revised manuscript which I find very interesting and have no further comments. If you can attend to the reviewers' points I am confident I will be able to accept the manuscript.

> We sincerely thank your review and handling of our manuscript. We have revised our manuscript based on comments from the reviewers. We have also checked and modified the reference list to fit the style of this journal.

Reviewer #1: I was enthusiastic in my reading of the original manuscript, and my enthusiasm has only grown with these careful and substantial revisions. I would like to sincerely thank the authors. There is nothing more frustrating than peer-reviewing a manuscript only to have your comments ignored. I appreciate the respect and thoroughness with which the authors addressed my comments and suggestions. I look forward to seeing this paper published with the full fanfare and acknowledgement it deserves. My remaining (minor) comments are below:

> We sincerely thank your review and helpful comments on our manuscript. We feel that our manuscript has been improved thanks to your comments. Based on your comments, we have revised our manuscript. We have responded to each of your comments in detail as follows.

1. I would include the scientific name in the title of your article

> As you suggested, we have added the scientific name in the title.

2. I would combine the first two sentences of your introduction to read something like "Male competition over access to females is central to securing breeding opportunities in many species".

> As you suggested, we have combined the first two sentences in the Introduction as follows:

L49-50: “Male competition over access to females plays important roles to secure breeding opportunities in animals [1,2].”

3. I would replace the word "animal" with "social" at L65

> As you suggested, we have replaced “animal” with “social” at L59.

4. The paragraph from L65-L85 is great!! Really concise but clear explanation of the knowledge gap your study is filling.

> Thank you for your helpful comments and warmful words.

5. I would revise the sentence at L89-90 to read "There is evidence of paternal kin-biased behavior in primates" for clarity.

> We have revised as you suggested (L82-83).

6. I would revise the sentence starting at L102 to read something like "Japanese macaques (Macaca fuscata) provide an interesting opportunity for the investigation of paternity success of non-resident males and their contributions to the production of within-group kin-dyads"

> We have revised as you suggested (L95-96).

7. L104 Is "bisexual" really the word you're looking for? If you're referring to multiple males and females mating with each other, you might be looking for the word "polygynandrous".

> As you suggested, we have used the term “polygynandrous” at L98.

8. I would generally rephrase L104 to read "They form female-philopatric multi-male and multi-female groups characterized by strong matrilineal affiliative relationships and a polygynandrous mating system"

> We have revised as you suggested (L97-98).

9. L110 "Noteworthily" reads a bit odd to me. I would remove.

> We have deleted “noteworthily” as you suggested (L103).

10. Has a high percentage of EGPs been previously recorded for Japanese macaques specifically? Or is L110-111 referring to other species?

> Yes, a high percentage of EGPs has been previously reported (Hayakawa 2008), whereas the EGP has not been assessed at an individual level.

11. Thank you for expanding table 1 :)

> We appreciate for your suggestion.

12. Methods overall are greatly improved and offer better detail and clarity!

> We appreciate for your helpful guides.

13. I have no comment on genetic methods as this is not my area of expertise.

> Ok, but thank you for reading even genetic methods.

14. Very interesting results. The discussion appropriately contextualizes the results within the limitations of the study. I appreciate the comparisons to other specific studies and species.

> We appreciate for your helpful guides and warmful words.

Great work, authors!

> Thank you very much!

Reviewer #2: Thank you for the opportunity to review this interesting manuscript. The authors set out to examine the reproductive success of non-resident:resident male Japanese macaques in a provisioned, habituated population. There is little information on non-residents in the published literature, so this represents a unique and important contribution to the literature. Additionally, the authors calculated the number of paternal siblings in the study group, which will aid in our understanding of how kinship influences social behavior. The authors have revised the manuscript and addressed the previous two reviewers' concerns in my judgement. I recommend publication following minor revision. I used track changes in the attached document to help the authors find places where I changed sentences or had questions regarding their meaning. I wish them the best of luck with future work at this site.

> We sincerely thank your review and helpful comments on our manuscript. Based on your comments in the attached document, we have revised our manuscript. We have responded to your comments as follows:

[A1]: I suggest this phrasing, because it is the variation in RS that is being explained.

> We have revised as you suggested (L52).

[A2]: I am unsure of your meaning here--I think you mean that you did not systematically collect behavioral data from these individuals.

> Yes, as you suspected, we meant that we did not record the presence of group members systematically. To clarify the meaning here, we have changed the term “quantitatively” to “systematically” (L130).

[A3]: You may explain this later, but are the NR males the same individuals across each of your study years? Or are new males coming as NR each mating season?

> As you suggested, the information about genetic sampling should be placed later. We have thus moved the sampling information later as follows:

L196-197: “Since we collected genetic samples for 19 candidate fathers, which included three of the four identified non-resident males and accounted for 60–70% of all candidate fathers”

We considered that the information about the number of non-resident males identified should remain here. Therefore, we have revised this part as follows:

L153: “We identified four non-resident males during the study period.”

There were both types of non-resident males. Several non-resident males came across years. Several new non-resident males also came in some mating seasons.

[A4]: I am unsure of your meaning here--I think you mean reproductively active?

> Yes, we meant the estrus capable females. The estrus capable females were explained at L215-217. For clarity, we have added “estrus” before “capable” at L259.

Attachment Submitted filename: Response to Reviewers.docx

10.1371/journal.pone.0309056.r004
Decision Letter 1
Santacà Maria Academic Editor
© 2024 Maria Santacà
2024
Maria Santacà
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Submission Version1
6 Aug 2024

Paternity success for resident and non-resident males and their influences on paternal sibling cohorts in Japanese macaques (Macaca fuscata) on Shodoshima Island

PONE-D-24-26360R1

Dear Dr. ISHIZUKA,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Maria Santacà

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

10.1371/journal.pone.0309056.r005
Acceptance letter
Santacà Maria Academic Editor
© 2024 Maria Santacà
2024
Maria Santacà
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
11 Sep 2024

PONE-D-24-26360R1

PLOS ONE

Dear Dr. ISHIZUKA,

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PLOS ONE
==== Refs
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