Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. xetdt nraeterfins yicesn h ubro aigprnr stersl fterhigher their of result the as are partners males mating do as of others recognized, number while well the are partners increasing (EPC) multiple rate by copulations reproductive with by fitness extra-pair potential mating their in affected engaging increase in be of to engage to males densityexpected individuals shown to population advantages some and been The strength why have pair-bond not. is and care, male question populations of intriguing intensity and example, The species for as, between of such substantially factors, understanding various vary our species EPP therefore other incomplete. and pair- of Four very yet, most Rates for exist is 2). However, (Table monogamy not <10%. far genetic does EPP simply of so of data frequency species rate paternity the seven the genetic method with only species, monogamous, classification for mammal genetically the reported living “mostly” study), on been as this depending considered has in be species, EPP) can used of mammal extra- definitions cases of partners, for (no phenomenon 9% systems mating 1 monogamy rare to mating Table very of up a of (see number constitute is mammals evolution monogamy which the and the genetic by birds while in influenced humans, monogamous role including is socially important or females an pair-living, and play in males (EPP) both paternities in pair selection sexual Since monkeys, Introduction titi dispersal, choice, mate not monogamy, Genetic is it both as render long words can maintain Key to as turn, helping in dispers- thus dispersal, unnecessary, This, sexes copulations opportunistic extra-pair both inbreeding. monogamy. even and prevent with choice genetic that mate to opportunistic, via diversity indicate avoidance was partners genetic inbreeding findings mating dispersal active sufficient choice, Our that generate mate found can via distances. further constrained, avoidance We varying inbreeding heterozygosity-based active or over related. relatedness- for ing not for evidence average evidence of show find on lack we not were the did Here Despite We mammals. paternity. choice. extra-pair pair-living mate of in cases dispersal about no known and indicated is choice ( extra- little monkeys mate However, in titi coppery system, incompatibility engage dispersal. that mating natal or might by between inbreeding individuals avoided inbreeding, interactions of be minimize the risk can monog- inbreeding and a socially Alternatively, constraints generating in copulations. these that constrained, pair escape is severely To reason be possible partners. can One between choice rare. mate extremely animals, is monogamy amous genetic mammals, pair-living In Abstract 2020 28, August 3 2 1 primate pair-living Dolotovskaya a Sofya in choice mate and monogamy Genetic emnPiaeCenter Primate German Research Primate Centere for Primate Institute German Leibniz Centre Primate German 1 hita Roos Christian , lcuoeu cupreus Plecturocebus 2,9 oee,i arlvn pce ihbprna ae oeta reproductive potential care, biparental with species pair-living in However, . 2 n chr Heymann Eckhard and , ,aemsl eeial ooaos sprnaeanalyses parentage as monogamous, genetically mostly are ), 1 Plecturocebus 1,3,4 3 mn arlvn aml  mammals pair-living Among . 1,2 P r common are EPP . 5,6 titgenetic strict  3,4,7,8 . Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. vi nreig nms aml,mlsaetedsesn e,bcuei oyyosmtn systems, mating females than polygynous to mates in males for because and competition intra-sexual sex, females stronger dispersing breeding experience between the males dissimilarity mammals, are in genetic males prevailing allows local are mammals, thus which enough most situations and generate In many to inbreeding. associations avoid sex-biased in kin be dissimilarity opposite-sex to genetic disrupts has of that them level dispersal between certain natal or above matings territory recognition) discussed by avoid kin good as ensured (through to a individuals, individuals be can choosing related related problem can between less closely of This trade-off avoidance with with risk mates. a matings EPC the related avoiding of in is closely either result engaging animals too by a pair-living with “actively” as in pair solved or choice might be mate individuals options, partner, of other constraints unrelated/compatible of the and absence from the arising In problems inbreeding. biggest the warblers, of reed great One and titis found blue not lemurs, was dwarf seals, fat-tailed fur as Antarctic lemur, such arundinaceus as dwarf species, such studied fat-tailed species, other some many (e.g., in in dissimilarity demonstrated while loci relatedness choice, mate MHC low rat, relatedness-based on and jumping based giant heterozygosity Malagasy be high e.g., to between shown optimize medius was to Cheirogaleus choice further mate move species, to many shown heterozygosity were partner’s females on based were gazella example, preferences For care, mating parental mammals. and increased that birds of as tits, species such various blue in benefits demonstrated in was direct heterozygosity on provide based to choice Mate likely al., more territory et quality be compatibility, Foerster good expected should genetic are 1999; or of and partners fertility irrespective heterozygous al., fitness addition, because higher et mates, In have heterozygous Coltman (2007). choosing to from (e.g., Kempenaers benefit in resistance also reviewed might expected proxies, parasite 2007) individuals is fitness al., and various mating et and success disassortative Ortego heterozygosity (e.g., reproductive 2003; this individual genes between survival, from fitness-related links as resulting some by heterozygosity at such indicated as dissimilar offspring fitness, or in offspring unrelated increase increase genetically An are that genes). posit mates heterozygosity heterozygosity MHC offspring choose and maximize so increased compatibility to will do as genetic that expected to expressed mate of are a expected benefits, hypotheses choosing (genetic) is related from indirect it benefit closely the EPC, individuals The also seek that but to offspring. benefits, or of fitness partner quality direct social genetic its its only to not matings maximize restrict to to chooses individual more an in Whether engaged partner social their lemur, with dwarf (MHC)-supertypes fat-tailed EPC complex the histocompatibility is major demonstrated more been sharing has effect this related which closely for more partner were partners social where indirect the gain by a to species provided As them bird escape benefits marmots, To allow various direct would in partner. benefits. of that related demonstrated advantage face genetic EPC closely been taking may a seek indirect still to might individuals and or while animals also incompatible care) inbreeding, benefits but genetically minimize paternal a paired, and (territory, to constraints once paired benefits these unavailable up can pair-living direct end choice become In may mate for mates individuals density, choice. choice result, breeding do mate low between in only and conflict limitations mobility Not low to a with related constrained. those be highly in EPC to especially be in could care, engaging females biparental females from to with and EPC benefits species males of gain for advantage to similar potential expected more One be be might will sexes competition both intra-sexual result, of a levels consequently, and, rates 14 hr eae xr hieb oigars reigcln ovstlreysainr males, stationary largely visit to colony breeding a across moving by choice exert females where , . amt marmota, Marmota ynse caeruleus Cyanistes Gr´ aNvse l,20;Hnsne l,20;Sheswe l,20;Sme,2005). Sommer, 2008; al., et Schwensow 2007; al., et Hansson 2009; al., (Garc´ıa-Navas et : 14 r ovrey iiaiy(rbbya dpaint oa ahgn,sonin, shown pathogens, local to adaptation an (probably similarity conversely, or, n meerkats, and eeoyoiywspstvl orltdbtensca ae,indicating mates, social between correlated positively was heterozygosity , 15,20 26 yoemsantimena Hypogeomys ipra a hw ob ucett vi nreigo ec a reach or inbreeding avoid to sufficient be to shown was Dispersal . . 12,13 7,11 uiaasuricatta Suricata u,t u nweg,teol arlvn amlspecies mammal pair-living only the knowledge, our to But, . nmmas h vdnei uhmr iie.I Alpine In limited. more much is evidence the mammals, In . 2 n uoenbadgers, European and , 21,24,27 P ae eefudt ehge npairs in higher be to found were rates EPP oee,i ean nla fdispersal if unclear remains it However, . 21 10,25 nAtrtcfrseals, fur Antarctic In . lentvl,“asv”inbreeding “passive” Alternatively, . hioaesmedius Cheirogaleus 10 . ee meles Meles 10 15–17 hssrtg has strategy This . hs animals Thus, . hr females where , Arctocephalus 22,23 Acrocephalus Finally, . 20 2 In . As . Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. l h ape nml n lowsteol niiuli u aae o hmw nyhdoefecal one had only other we all for whom did for we like dataset sample our another among using in loci errors loci individual typed the was the of for only it control number of the that not minimum one was could suggest individuals. the we At only also had Therefore, can and offspring collected. we fathers. this animals sample so likely Unfortunately, sampled heterozygous, most error. was the genotyping as genotyping offspring or all a the 8 dropout chr08a), of Group allelic (chr07a, result score from of loci a resulting Delta two male likely and was other homozygous, adult parents) group, at was the candidate The the error, offspring likely and the of unassigned. most (chr09a), two male male remained mismatches for adult this paternity with ratios social the case, both likelihood 9 with genetic the one indicating between in as mismatches In zero, difference identified offspring three (the groups. were (17 had Cervus fathers family paternity by 10 social respective calculated assigned Group S1), their of Table from Supplementary cases in offspring 1, all offspring juvenile Fig. In all group; EPP. of per of offspring fathers cases 5 any to 1 indicate groups, not did analyses Our monogamous? genetically titis Are expected as via disperse, avoidance to care. inbreeding sexes biparental active for both Results with high for predicted mammal We especially evidence territorial be find pair-living to choice. to expected mate a is expected heterozygosity-based genetically from inbreeding we for be of to and/or titis, risk them choice as consistent the predicted mate we Since such Given EPP. titis, analysis. species of coppery in rate genetic pair-living care low and/or long-lived spatial male very relatedness- of performed a relatedness levels have and of genetic high or and males compared monogamous evidence that bonds and we for pair loci sex-biased, females strong microsatellite tested living, is adult developed wepair we dispersal in study, newly Second, if patterns 27 this monkeys. see diversity of EPP In World to and set mammals. of Finally, New a choice. in rates to using mate monogamy the titis applied heterozygosity-based genetic affect coppery universally and of to exhibit be social system shown that of can mating characteristics evolution taxa the two the mammalian examined bonds, on few first light very pair shed the strong therefore, of and may, one care are male mammals Titis of the in system. by level mating exclusively high almost genetic carried both the is infant is (the characterized monomorphism care wild sexual be male a and of territoriality, level in father), high dispersal social exceptionally and an choice bonds, mate pair long-term system, mating genetic monkeys, the and titi of coppery study of comprehensive population a present monkey, we Here, owl Azara’s dispersal. monogamous in genetically bias female-biased be the sex as no such or californicus mammals, little some have in to male-biased true expected be are azarae to Aotus pair found dominant was a This by monopolization reproductive 26,28 olwn h aelgc aml htmt ooaosyo oprtvl ihhg eesof levels high with cooperatively or monogamously mate that mammals logic, same the Following . Cheracebus rscal ooaosgetrwietohdshrew, white-toothed greater monogamous socially or , 29,30 hr ohsxsdses,o oprtvl reigmekt,weedsesli nyslightly only is dispersal where meerkats, breeding cooperatively or disperse, sexes both where , 3 h xmnto ftermtn ytmadtepoiaemcaim fismaintenance its of mechanisms proximate the and system mating their of examination The . xii lotalteeeet fte“ooaypcae,sc spi iig strong living, pair as such package”, “monogamy the of elements the all almost exhibit ) oee,i te aml,eg,gntclymngmu aionamice, California monogamous genetically e.g., mammals, other in However, . 31,32 . lcuoeu cupreus. Plecturocebus 3 33–36 iimnes(genera monkeys Titi h nymsigcmoetwihhsytto yet has which component missing only The . rcdr russula Crocidura Callicebus ipra a on to found was dispersal , , Plecturocebus Peromyscus , Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. olo 2fmlsad1 ae) ieie efudn vdnefrhtrzgst-ae aecoc,as choice, mate heterozygosity-based breeding for pairs, evidence 10 no = of found n relatedness we 0.565; between Likewise, = difference p males). -0.021, no 12 vs. was and (-0.048 females There pairs 12 mating of choice. generated randomly pool mate and relatedness-based pairs for mating real evidence no heterozygosity? found all or We between relatedness Colony relationships on with full-sib based assignments. for choice confirmed parentage support mate correct and strong Is confirming software yielded groups, mother-offspring also Cervus same known Colony of the in priors. set from the level the offspring when from change confidence excluded not 95% did was assignments pairs a The The juvenile our with it. S1). Table with father. in group’s (Supplementary made haplotype software genetic female the mtDNA were the other a of as assignments No shared mother was indicated or All mismatches. replacement was genetic offspring allelic juvenile this female the 11 for this of family as mother had of case likely identified their and father inferred most not haplotype in social the One mtDNA was as offspring the identified group). 4 all was share per Group sample of not offspring of did mothers 5 female they genetic to adult offspring; 1 as the this groups, identified that as 7 were assumed detected, in we seven offspring loci, mothers, (17 other social groups the sampled by given eight parentage error. Of of genotyping homozygous not a likelihood was to high daughter genotyping the or due the chrXa; dropout was considering locus allelic mismatch but at allelic of mismatch result of locus a a cases this had likely two 9 most at chr10a. was Group only locus this from found at dyad locus, Father-daughter mismatch we this a paternity, at error. had homozygous unassigned 1 was the Group daughter of from the not dyad Since case Father-daughter likely the S1). most Table in home (Supplementary mismatches was mismatches The three territory the established range. from newly home Apart this its because estimate line reliably as later. depicted dotted to shift is as data to 14 depicted GPS Group bound is enough of and have 11 range permanent 95% home not Group the The did of and using (ESRI). we circles range estimated 10.6 of were because Desktop colors groups ArcGIS ellipse study The with dotted of respectively. method circles ranges groups. offspring, density smaller Home study kernel male respectively; fixed within haplotypes. and males, mtDNA female individuals and different represent sampled females represent outline for squares adult dotted parentage represent with and outline squares continuous haplotypes, and with mtDNA squares ranges, and Home Circles 1: Figure 4 Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. ae eg,Brlie l,21;Nmee l,21;Pti epnes 98 u e oa,Yco,Da of Yoccoz, reports Cohas, anecdotal see only but most titis, 1998; in In Kempenaers, individuals 2011). animals & neighboring Chivers, mated Petrie the & the 2019; to Binh, intense al., with Roos, attributed et experience copulate Kenyon, are Allain´e, Nimje 2006; not individuals EPP & 2013; do and mated Goossens, al., floaters Silva, expected, et system, that intuitively Barelli social indicate (e.g., be their species cases might mammal as of and often aspects as bird all of sexes other in importance both many of the and titis wide mammals floaters for to a from and evidence over competition accumulating similar birds intra-sexual ranging is very both individuals There of are non-territorial groups. Another dynamics who solitary little natal residents. population very floaters, their same-sex in have with from the groups floaters mating dispersed from would study having be aggression individuals our after mates, could risking extra-pair area of ranges, EPC find home ranges obtain to neighboring home and to the 1), way The into Fig. intrude data; too. to unpublished prevent limited, need (0–4.7), to likely average enough on are (1.4% effective EPC borders overlap and for territorial easy the opportunities guarding at The mate duetting make and should together four displays sleep coordination just other, visual and on each EPC. joint proximity from based meters frequent of was few level in gibbon a high within engage Bornean day of and on the evidence of night study no most (the at spend with size mates mammal pair sample groups pair-living pair-living, adequate consistently seventh family an the four with and from study species infants a primate active in second both found the render EPP only to are natal males titis population, and Coppery heterozygosity-based study in females our or mates between unnecessary. in pair dissimilarity EPC relatedness- that choice, and genetic for suggests mate avoidance of finding evidence inbreeding via level This find avoidance sufficient inbreeding relatedness. not generates average active did low dispersal for had also evidence We population of study absence evidence our the find mammals. not population. Despite pair-living did in study we choice. as studied mate our monogamous, been genetic in rarely mostly are EPP has monkeys dispersal for titi coppery and that choice demonstrated 0.342). mate we = Here, system, p mating right-tailed between in dyads, link distances The 91 spatial = and n 0.048, (Supplementary distances classes = haplotype for distance correlation mtDNA all significant (Mantel dispersal between for either not correlation that zero significant was overlapped The suggesting not values distances was S1). r population, spatial females autocorrelation study Fig. and of 2, our CI genetic Table % in between Materials 95 correlation structure the as The genetic sex, spatial either opportunistic. in for likely 0.216 evidence most females, find is in not (0.184 HL did heterozygosity We 0.699), 0.438). mean = = or p p bootstrapping) test t-test by permutation paired obtained males, males, in 0.054) permutation 0.029 – males, females, in (-0.048 in interval 0.924 (0.027 females, diversity in nucleotide (0.945 relatedness mtDNA diversity betweenmean differences 0.766), haplotype significant = mtDNA no mean p were There in test other? males distances. the and similar than females dispersed sexes further adult both had disperse that others sex indicate results while one Our does 9), and 5, disperse 4, sexes Groups second-degree 11). both (e.g., be 1, Do haplotypes Groups to related (e.g., found mtDNA closely haplotypes partners same related had the the distantly some were only shared pair mates: mates one pair pair in between the similarity Only of 6, 1). none (Group Fig. and (Wang’skin 1, -0.033, relatedness Table choice, p averaging mate (Supplementary pairs, low, via haplotype 10 generally avoidance = inbreeding was active n partners for -0.527, mating evidence = of (r lack mates the Despite pair between correlated significantly not 0.118). was = (HL) loci by homozygosity Discussion r .8) h tN altp ewr Fg )soe ocerpteno haplotype of pattern clear no showed 2) (Fig. network haplotype mtDNA The 0.285). = r -.1 nfmls 006i ae,ma ieec 000 yn ihnte9%confidence 95% the within lying -0.040, difference mean males, in -0.056 females, in (-0.013 37 al ) h bec fEPi ii sntuepce,a hyare they as unexpected, not is titis in EPP of absence The 1). Table , 43,44 5 oee,teeiec rmAaasolmonkeys owl Azara’s from evidence the However, . 42,43 o xml,i zr’ w monkeys owl Azara’s in example, For . 36,38–41 r between ) This . Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. ieo 8osrn,wihi icl oaheei esnbepro nasceieabra rmt with primate arboreal year. our secretive a sample in a once a rate in only need EPP period births would 16.2% reasonable singleton we is a giving EPP, in and there of achieve size pairs that 5% to sample in imply least the difficult living at does history, is is to life and n which interval slow size and offspring, confidence EPP, sample 58 the of of the down frequency size of narrow the To product 1–(1–x) is population. = a x study (0.95); y is offspring as limit found extra-pair calculated been confidence has one 16.2%, This EPP least be no at (assuming will level producing confidence) EPP of 95% possible weaned. 2 maximum with been offspring, ca. estimated 17 had within of and at months juvenile happened size time 6.5 the have sample the must the ca. after given replacement of groups, lasts Second, body female most the titis its the own following in that their on started Lactation assume we on based 1995). we walk before old al., Therefore, to months months et nursing. start Jantschke 7–8 female titis months: be the as (juvenile 4.5 father. see to identified independently ca. genetic walked estimated not of the it was was as age that juvenile indicated 4 the fact was the Group male the group, of adult and this that the female no size following while indicates adult and offspring, data started The collection juvenile Our we group’s population. sample history. When the demographic genetic study of its the our mother reconstruct before genetic in not the in shortly happen could even habituated do we monogamy only replacements it, genetic was in adult from present 10 deviations were Group apparent offspring As the deaths) older EPC. to (presumable leading of disappearance offspring, absence the are their immigrants the replacements after and same-sex Adult vacated parents group. by positions biological a in occupied breeding of replacement genetic the being male the with not a in adults indeed of titis, rate of is result EPP in father the the happen social be case, the could to it this that case paternity known confidence, In assume this we 10), with male. offspring), (if the paternity extra-pair (Group Alternatively most of intra-pair unsampled 6%. the father offspring an nor be as by would extra- one identified sired population exclude neither was for was study as fully sample offspring our First, classified our cannot this be population. from that we could male possible study group), case other remains our per any this nor generations While in father father. offspring group rate social likely the 5 neither EPP for to as low fathers unassigned, up genetic a remained groups, as of identified 9 were possibility in fathers percentage the the social born the for the offspring paternities and accounting (17 assigned ha) possibly offspring of (5.0 2020), cases (Van all smaller Fiore, yet in average published and Although on (Fernandez-Duque been were (4.8%) individuals/km not ranges larger (57 has rate. home was EPP population data the overlap higher this these range population, of although home study density offspring, our of The 16 of abstract). of that conference size than 2016b, sample al., a et in titis Belle EPP of of populations density cases The undisturbed of (1966). for three population Mason reported a of values bigger study for of S1), the Table range that (Supplementary in average ha groups the 7.2 nine within by was was inhabited group population 57–59 ha one study 6.9 of our of range of fragment home forest the entire of the size than average the and data), hed 56 beavers, Eurasian in (previously e.g., encoun- demonstrated, the was making densities rates 8,45,54,55 likely higher EPP less the and EPC with density consequently, density, and, population by individuals between affected also ters are including EPC withholding for risks retaliatory Opportunities the the individuals. females, with neighboring males for costly, the by and, be diseases with care pair transmitted might parental EPC sexually between animals, of than acquiring coordination neighboring obtain of to probability and or higher proximity easier floaters the not of with probably levels whether are high EPC, floaters the Furthermore, the given with However, EPC too. mates, populations, titi in present exist intruders by replacements o oprsn h ouaindniya u td iewsetmtda 4individuals/km 34 at estimated was site study our at density population the comparison, For . hsrltvl o est ieylmtdteopruiisfrEC tsol emnind however, mentioned, be should It EPC. for opportunities the limited likely density low relatively this ; oal,teol ulse eodo P nttscmsfo ouainof population a from comes titis in EPC of record published only the Notably, . .moloch C. iigi itre aia ihecpinlyhg est f46individuals/km 406 of density high exceptionally with habitat disturbed a in living ) lcuoeu discolor Plecturocebus 51,52 . 49,50 u ie h iclyo eetn otr,i spsil htte are they that possible is it floaters, detecting of difficulty the given but , rmudsubdhbtt rlmnr nlssreported analysis preliminary a habitat, undisturbed from 33 elcmnscncet rusta ontconsist not do that groups create can Replacements . 6 53 h oiierltosi ewe population between relationship positive The . atrfiber Castor 17 hr steprobability the is y where , n nmn idspecies bird many in and , lcuoeu ornatus Plecturocebus 62 n eddnot did we and , 2 a higher was ) 2 (unpublis- 63 2 . Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. n ftenihoiggop.Tecoetrltv fti eaewsteautml fGop4with 4 shared Group also any of she have male whom from adult with not the half-sibling), dispersed did was and not female female unrelated had The this between mate, level of his her female. relatedness relative of to unlike a closest unknown case adjacent she, to The an observed area that (corresponding direct with groups. unoccupied directly 0.156 indicating neighboring the 11) an one animals, the with (Group to In sampled of line moved pair any the in 1), a among population. Group are formed kin study of they later centersfirst-degree the offspring However, and home-range oldest of preliminary. group between (the structure as natal male distance kin treated subadult maximum the be a the distances. and should dispersal, varying with results dispersal over confined, migrated these of was sexes m, observation study spatial both 3200 There our that of only mean suggesting 3). of absence of and 2, males, diversity scale the haplotype and (Fig. mtDNA geographic by network females both As haplotype as in indicated mtDNA sexes, similar as between the were distances in opportunistic, dispersal relatedness clustering in likely geographic difference obvious of most (squares) no lack was was males the dispersal and and structure population, (circles) genetic haplotypes study mtDNA females different our adult represent In squares of and haplotypes circles of mtDNA colors and The kinship study. this ranges, in Home sampled 2: Figure such in occur avoid occasionally will to that sufficient levels tolerated unnecessary inbreeding be be low choice may and will mate evolve, systems dispersal via to avoidance fail situations, might inbreeding most mechanisms active pair-living discrimination in in rendering most that reviewed low, in suggested 2005; relatively found Sommer, kin been was 2008; 2020), has al., al., It et et Schwensow inbreeding 2009). Leedale 2007; al., 2007; al., et al., et Jamieson et Hansson Hoffman 2009; (e.g., al., (Garc´ıa-Navas pair mammals et species grey and the e.g., birds case birds, some and in one mammals in of Only populations tits, other 2). (mean many related Fig. in not demonstrated S1, wolves, average was Table avoidance on via (Supplementary inbreeding with avoidance were active kin haplotype inbreeding population second-degree mtDNA active study were choice for same our mates mate evidence the in heterozygosity-based of or shared mates absence relatedness- pair never the for the despite evidence choice, Interestingly, find mate population. not study did our we in predictions, our to Contrary au caeruleus Parus ai lupus Canis 24 ydsutn ls-i soitos ipra a aetepoaiiyo noneigclose encountering of probability the make can dispersal associations, close-kin disrupting By . rtcfoxes, arctic , 24,64,65 66 . nfc,atv nreigaodnevamt hie lhuhdemonstrated although choice, mate via avoidance inbreeding active fact, In . upslagopus Vulpes r .8.Lwrltdesbtenmtn atesi h bec of absence the in partners mating between relatedness Low 0.285. = ra edwarblers, reed great , 7 coehlsarundinaceus Acrocephalus 66 nsc ae,kin cases, such In . r 003 and -0.033) = n blue and , r = Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. einvcos h oosrpeetn tN altpsmthtoeue nFg ,2. in 1, constructed Fig. groups, in study used those our match in haplotypes found mtDNA representing haplotypes colors mtDNA The all vectors. of median network joining median PopART A 3: Figure further migrate unrelated). first-degree others are adult ranges), home by area 1–2 (indicated study by area the separated the in or adjacent in individuals (Fig. either many stay population are study (as individuals that the dispersing ranges of home some structure occupying while kinship kin that The suggested S1). further Table 1) (Supplementary haplotype mtDNA same the 67 h ubro ac ak niae h ubro uain.Bakndsidct inferred indicate nodes Black mutations. of number the indicates marks hatch of number The . 8 Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. h td a odce tteEtco ilgc ubaaBac ntenrhesenPrva Amazon Peruvian north-eastern the in Blanco Quebrada Biologica Estacion the (4 at conducted territory. was study the The of population quality study or size and on the site based or is Study choice condition level. mate body any if at loci, examine titis MHC in to in have occur Methods variation will not e.g., studies does choice as, continuous future mate mate such titis, in heterozygosity-based that factors, in via inbreeding and mean other patterns avoidance not relatedness- of mating does inbreeding of levels understand course, active absence and better of To the for population, patterns Finally, study mechanisms mating our populations. the compare in choice isolated lack to dispersal or investigate examine necessary indeed further fragmented to be titis to vs. needed will if and be it titis examine coppery will discrimination, to of choicekin size not particular, populations mate is sample In different active it larger in render as monogamy with patters. to long genetic studies low of as sexes Future had extent further dispersal, opposite the unnecessary. still between We opportunistic choice, copulations dissimilarity even mate extra-pair genetic that copulations. via and sufficient indicate avoidance extra-pair create results inbreeding Our can for active guarding constrained, mates. no opportunities mate and pair exhibiting effective choice the between enabling despite mate population relatedness bond limiting titis, study pair system, density our coppery strong mating in that a population titis between showed of coppery low result link that a showed relatively the We as examine likely and primate. monogamous, to pair-living genetically a first mostly of the are population rendering wild is low, a study is in current inbreeding dispersal for the potential up, the Summing and shown unconstrained were is partner habitat species, unnecessary. this social one EPC in their in dispersal with demonstrated that only MHC-supertypes EPC suggestion knowledge, more more our sharing in to engaged females was, to where relatedness strategy lemur, mate similar dwarf pair a avoid and fat-tailed mammals, to rates pair-living species way EPP In bird potential between often. many another relationship Positive in individuals, EPC. unrelated demonstrated in with was engaging mating through preferential tolerated. is and occasional inbreeding presumably dispersal kin, is to second-degree and were addition populations ensuring mates In such unconstrained, pair likely in where most occur case was one still dispersal tits, by can and indicated inbreeding great undisturbed, As was in correlation habitat avoidance. a the inbreeding (e.g., demonstrating site, passive level studies study by our inbreeding At indicated mechanisms and further avoidance 2008). was inbreeding distances risk active dispersal inbreeding for and between need dispersal the was habitat between without link avoidance by but The inbreeding dispersal unconstrained sifakas, unconstrained for golden-crowned is and from dispersal it dataset structure even unconstrained empirical as that on of long indicating based importance study salli studies as simulation The other inbreeding, a from in prevent factors. supported evidence to other the sufficient or with be fragmentation line can in dispersal are preliminary, opportunistic although results, These curdbtenOtbradFbur n nyoeocre nJn SplmnayTbeS) sthe As S1). Table (Supplementary June years in 2–4 occurred of age one year the only a at and once disperse February infant offspring and single October a colouration, between to and occurred human shape birth tail give of size, typically in- presence body We Titis the study. of combination marks. to this the natural during habituated from on habituated and been continuously based were shape, animals had collected groups genitalia study 1 were other the the Group samples all 1997; identified 2019. genetic since dividually September and intermittently until month, studied study and per in observers the days conducted of studies 2–3 behavioral beginning for to the monitored subject were also were groups 2018 1–7) the June–December (Groups which and of 2017 seven June–December 1), Fig. S1, Table mentary ° 1S 73 21’S, hwn hthg eeso ubedn a emitie napplto yacmiaino social of combination a by population a in maintained be can outbreeding of levels high that showing , ° 9W nJn 07–Spebr21.Suyidvdasblne o1 aiygop (Supple- groups family 14 to belonged individuals Study 2019. September – 2017 June in 09’W) 14 norsuypplto,teasneo vdnefrEPfrhrcnrsour confirms further EPP for evidence of absence the population, study our In . 7,10,11 33,57,72 u arlvn aml ontse oueti strategy this use to seem not do mammals pair-living but , h eirei u td opie pt eeain of generations 5 to up comprised study our in pedigree the , 38,70,71 9 33,57,72 ewe h eid fbhvoa aacollection, data behavioral of periods the Between . norsuypplto,ms ftebirths the of most population, study our In . au major Parus zli n Sheldon, and Szulkin : rpteu tatter- Propithecus 68 . Posted on Authorea 28 Aug 2020 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.159492953.34696224/v2 | This a preprint and has not been peer reviewed. Data may be preliminary. sn ie egn i 2wt hXDA(luia de nteMSqsse Ilmn) Sequencing (Illumina). system MiSeq sequenced the and on pooled added then (Illumina) and DNA using PhiX nM quantified with 10 were v2 to Kit diluted molarities and Reagent were and BioLabs) Miseq Libraries England sizes Technologies). using (New Fragment (Agilent Kit Fisher). 2100 Cleanup Bioanalyzer (Thermo DNA a Fluorometer & indexing PCR Qubit Monarch each using the with of quantified with done mM) purified were were (0.5 PCRs libraries mL Full-length Indexing 98 1 product. 62 at ReadyMix, PCR at total Hotstart step purified annealing a HiFi ng denaturation with Kapa 100 (Roche) initial and 2x Kit an barcodes) mL PCR sequencing individual 12.5 ReadyMix prepare (containing Hotstart containing To primer HiFi mL Fisher). three Kapa 25 (Thermo of using of Fluorometer product PCRs volume (New PCR Qubit indexing Kit each Cleanup using performed DNA of we them & (or PCR libraries, quantified Monarch product and the PCR with BioLabs) multiplex products England pooled each the of purified mL reactions), multiplex multiplex 5 total The separate the pooled details). for we as for amplification, same Following Materials the were Supplementary amplified reactions (see additionally multiplex we separate reads three cases, more chr08a–chr12a,reaction. for these chr01b–chr07a, yielded conditions pools: in PCR usually primer and reads; following method reactions sequencing the this with of reactions as number multiplex chr12b–chrXa, separate low due three yielded times homozygosity in loci loci three false the prevent 27 reaction To multiplex all controls. each with non-template repeated each reaction with we of together dropout, mM gels allelic were (0.2 agarose to Amplifications pool 1.5% water. primer on RNase-free checked of of were mL mL 10.5 1 and DNA) 57 Mix, total total 95 at Master a ng at with Multiplex 200 denaturation (Qiagen) initial 2x (ca. Kit with extract PCR mL performed DNA Multiplex 12.5 of Qiagen containing mL the of 1 and using World primer), end PCR mL New multiplex 5’ 25 single to the a of in volume to applied loci sequences 27 universally all nucleotide simplify amplified be To adapter We added can S3–4). we Tables that primers. sequencing, Supplementary loci by locus-specific and the genotyping microsatellite Materials for Supplementary di-repeat preparation in 27 library described of are (details set monkeys monkeys new titi a for established loci microsatellite measured published was As extracts the of concentration genotyping DNA Microsatellite 10; kit Fluorometer buffer. Qubit Group stool elution a NucleSpin˜a DNA of and Macherey-Nagel mL GmbH) offspring the 50 Biotechnologie Fisher). one using PEQLAB in (Thermo (ND-1000, feces except DNA Spectrophotometer of animals the NanoDrop mg a of all 200 using elution for ca. final individual from a per details) with more samples Germany. for two to them Results least stored shipping see the and until (at Germany) necessary, dried DNA Karlsruhe, when We extracted Roth, beads defecating. We (Carl silica beads seen the gel was replacing silica individual temperature, containing ambient identified tubes beginning at falcon an years. the mL after consecutive in 15 several immediately in habituated from too samples were collected offspring defecations that were from groups their samples we samples those groups Fecal thus collected For some we and for members. humans, period, young group of study the very all presence the or the from still did of samples) to samples were either habituation collect obtain groups, differential groups offspring could to not other we family the due could Five before Also 14 because group). detected. disappeared in collected be per had to they offspring living be diminutive (or 5 not individual) period to could per study (1 the samples groups samples during family (3-15 offspring 9 have individuals of not offspring 41 putative from 18 samples including fecal collected We extraction DNA and collection sample Fecal S1). Table (Supplementary group per offspring ° o . i,etnina 72 at extension min, 1.5 for C ° o 0scadetnina 72 at extension and sec 30 for C ° o 5sc olwdb ylso eauaina 98 at denaturation of cycles 4 by followed sec, 45 for C ° o i n nletnina 60 at extension final a and min 1 for C ° o 5mn 0cce fdntrto t94 at denaturation of cycles 40 min, 15 for C ° 73–75 o 0sc n nletninse t72 at step extension final a and sec, 30 for C 10 eeldurlal eut o u td pce,we species, study our for results unreliable revealed 76 nsm ape,tettlmultiplex total the samples, some In . ° o 0mn C products PCR min. 30 for C ° o 0sc annealing sec, 30 for C ° o 5sec, 15 for C ° o min. 1 for C Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. aafrteXlne ou hX a sdsprtl omnal hc o lei imthsbetween mismatches allelic for The check sexes. autosomal manually both as to for way analyses. loci separately same parentage autosomal the used the 16 in was in of analyses offspring chrXa set the and the locus in parents using X-linked treated candidate performed the be were cannot tests for statistical and data following males the in all haploid loci, are loci X-linked As 4.5.4 analyses SeaView Statistical in Se- assembled Biosystems). and ( (Applied edited 1.8 Kit manually 4Peaks Sequencing 3130xL and with Cycle ABI checked BigDye an were the on sequenced electropherograms and and quence primers BioLabs) amplification England (New both Kit using Extraction sequencer Gel DNA Monarch the with purified 72 at extension final 95 vol- a at total denaturation a of cycles with 40 reactions min, PCR GenBank. in μ available monkeys primers World 30 using New of region of ume control genomes mitochondrial mitochondrial the of ba- of sis the I sets on region two designed hypervariable these newly 5’-AGGTAGGAACCAGATGCCG-3’, the from and 5’-TACCTCGGTCTTGTAAACCG-3’ at set. results individuals data all the one reduced genotyped Since data, We the of excluded. for chr01b sets only genotyping two results locus (mtDNA) further using with DNA all Mitochondrial analyses one mismatches present any further another we show and all substantially, not differ did loci ran locus not of we the did set below), As full (see alleles. size. the dyads null sample of with mother/offspring evidence small known showed and/or HWE, also the group from chr01b, for study departed loci, two chr21a, a these and in of chr01b relatives analysis. One loci, of this Two presence in HWE. the adults in included was to only population due we the likely species, that monogamous indicated 2.2.5 in analysis Micro-Checker especially The using analyses, stuttering genetic and population dropout bias allelic 2.2.2 alleles, PopGenReport null number with of mean presence the the and (Supplementary average), for (chrXa) on loci 78 locus loci all (16.8 X-linked checked loci one We 8.9. 14 and was of minimum autosomal locus a 17 per analysis. at including alleles genotyped further were of loci, from animals to excluded 18 All proved were or of S5). and chr16b) Table consisted chr11f, chr13b) (chr06b, set chr12a, animals were chr10b, final study reads chr04a, our The if <100 in chr02b, amplify alleles with (chr02a, to accepted monomorphic Alleles failed consistently be we either individual. Additionally, nine per loci, to and obtained 27 reads. Of and sequences genotypes 250 primer results three of the least the cutoff in at validate a called. in positions to not used reads “wobble” checked match We >100 contain manually not CHIIMP. yielded that do were by they loci that CHIIMP processed sequences those by incorrectly all for called are removing calling alleles then sequences allele the and All automated querying sequences, correct file, stutter attributes. sequence as MiSeq locus such each the artifacts, for using PCR etc.) processed potential length, then for sequence and counts, software (read we Reporter attributes relevant mistakes, MiSeq pipeline laboratory using individual. analysis for demultiplexed per CHIIMP 2– control were the genotypes To samples from four the field). individuals least sequencing, the at most After in assay to identified genotyped sexing leading be twice, we PCR-based not sample field, could a each further sex used the genotyped whom for also in for used We individuals animals were young of reads samples. reverse misidentification independent control. the possible 3 quality Only for MiSeq cycles. for control read used To only reverse were 251 reads and forward forward while 51 analysis, with performed was fec rmradc.10gttlDA Cswr efre ihiiildntrto t95 at denaturation initial with performed were PCRs DNA. total 100ng ca. and primer each of M easse ad–enegeulbim(W)adcluae bevdadepce heterozygosity expected and observed calculated and (HWE) equilibrium Hardy–Weinberg assessed We . μ otie itema 00(eerf) xrato ue,01 Mo ahdT,0.33 dNTP, each of mM 0.16 buffer, reaction 1x (Genecraft), 5000 BiothermTaq U 1 contained l ° o i.PRpout eerno %aaoegl,ecsdfo h e n then and gel the from excised gels, agarose 1% on run were products PCR min. 5 for C 79 ic h rsneo aiysrcuecncuedvain rmHEand HWE from deviations cause can structure family of presence the Since . 76 h HIPppln al lee yfis rdcn nqesqecswith sequences unique producing first by alleles calls pipeline CHIIMP The . ° o i,anaiga 58 at annealing min, 1 for C 11 80 l altpswr 6 plong. bp 567 were haplotypes all ; https://nucleobytes.com/4peaks/index.html ° o i,etnina 72 at extension min, 1 for C 77 ocnr eotdsx(n osex to (and sex reported confirm to ° o i and min 1 for C ° o 2 for C ) Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. ,wospoel a enrpae eoetesuypro,adteautfml fGop9 h was males who among 9, and Group females of among female Relatedness adult sampled). the be be and not not period, could could study but that Group the females period of before two female study adult replaced plus the (the analysis, been offspring during their this had present of in haplotypes supposedly the males who from adult inferred 4, were 12 haplotypes and whose females but sampled adult genetic haplotypes, from sampled function mtDNA available 12 R of in diversity 2016; included implemented nucleotide diversity al., test and the permutation et haplotype a compared MtDNA (Alexander using we males. compared and and sexes, females calculated between was adult among differ heterozygosity distances and relatedness, dispersal if examine To de- analysis. value correlation patterns a Pearson homozygosity Dispersal 3.1 (HL), two-tailed (4) GENHET the a loci function to used R by we locus in mates, homozygosity each implemented pair variability, calculated of between allelic we contribution their heterozygosity, levels the on heterozygosity individual weights pending individual estimate that compared To we measure pattern, microsatellite-derived mating mates. heterozygosity-based pair from any show between male titis subadult if oldest test the To and adults choice sampled pool mate breeding all Heterozygosity-based the included the (3) and This to pairs, compared mating males. real then 12 ten is 6. and included distribution Group females sample obtained 12 Our iterations The 1000 of pairs. over consisted iteration. mating pools each (2001). real each breeding to with male of for al. respect and relatedness values (1993), et with female averaged random relatedness Casteele from is al. pairs the de mating mating Van averaging the et generating if and and Li by pairs (1999) done mating of Ritland is of estimator relatedness this and STORM expected relatedness; Lynch the the in in using calculates randomly program described pairs implemented the and method Then, mating estimator real the real between using relatedness of weighted relatedness pairwise locus relatedness compared the we the individuals, calculates using related STORM partners with mating mating avoid generated titis if test To of (with set choice loci respective mate autosomal the Relatedness-based the (2) 16 test without of To Cervus. and set using mothers with calculated the them. candidate twice, pair, for nursing 9.9x10 of parent analyses probability was seen set the non-exclusion the excluded) were The Combined ran of chr01b they we beginning pairs. offspring because period. estimates, seven the mother-offspring For known sampling parentage in known offspring. were the our group candidate mothers of of plus with natal the haplotype males reliability end his mtDNA S1), adult the from their Table sampled shared by dispersed that (Supplementary all offspring had females included adult that sired fathers size all have 6 included candidate sibship population. Group could a of study from and and our set polygyny, male in study the group female subadult pairwise analyses, family and oldest Colony than per male the and offspring rather 0.01, of Cervus of group number both average rate maximizing For by the error and as individuals an calculated among individuals used 1.6, parentage we of of and analysis, prior clusters this sibship different For inferring expected of pedigree, likelihoods. and likelihood observed full the between a correlation 2.0.6.5 reconstructs comparing Colony highest Colony used we the Cervus, Additionally, showing Unlike relaxed loci. of simulations, 90% set in 0.01, our Relatedness for 1.0 of best values fathers. related rate and performed package simulation error mothers it candidate R an the of because the offspring, relatedness during 100,000 with for generated accounted of calculated and simulation thresholds was level, a confidence statistical used strict on 95% we and analysis, based Cervus parentage For assigns analysis. 3.0 and Cervus parents using candidate assigned was Parentage analyses Parentage (1) -5 o h rtprn,3.4x10 parent, first the for https://github.com/laninsky/genetic_diversity_diffs 81 evscmae ieiodrto ftetoms likely most two the of ratios likelihood compares Cervus . 82 sn agsestimator Wang’s using 12 -7 84 o h eodprn,ad9.0x10 and parent, second the for ovrf aetg sinet rmCervus. from assignments parentage verify to r 83 89 hsetmtrwschosen was estimator This . ots fH scorrelated is HL if test To . diversity -12 85 i 1.0.6 diff First, . o the for .We ). Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. 0 enos .D ere .Wyd eae aemltl?Arve fgntcbenefits. genetic of review A mulitply? mate females do Why M. Petrie, & D. M. in Jennions, selection. sexual and Rev. investment Parental L. R. 1972). 10. Trivers, (Aldine, 136–179 B.) Campbell, (ed. L. 9. Brouwer, paternity family extrapair monogamy bird predicts mates social single between to a similarity leads Genetic Cicho´n, infanticide M. & Male M. S. S. 8. studies. Drobniak, Shultz, A., bird & Arct, of M. meta-analysis I. a R. Dunbar, — D., mammals. Q. in Atkinson, 7. monogamy C., Opie, social of evolution The primates. H. in T. mammals. Clutton-Brock, in & paternity D. 6. Lukas, extra-group of correlates Ecological in T. 341 monogamy Clutton-Brock, genetic & of K. 5. Isvaran, Correlates G. T. Schurr, Sci. & Biol. L. P. Babb, E., 4. Fernandez-Duque, monkeys. M., owl females. Huck, Azara’s species and from between males insights variation (2014). in explaining selection mammals: Sexual monogamous birds: T. socially in Clutton-Brock, paternity Extra-pair B. 3. Kempenaers, & M. Petrie, 2. populations. and unrelated. as 1. categorized were r values with r dyads lower for with assigned References Dyads was dyads) dyads). uncle-nephew half-offspring or simulated half-sisters for as r such assigned genome, was the of categories) two 25% these r between with distinguishing dyads without to parent-offspring, and on (full-sibling based kinship conservatively assigned R was in Kinship groups permutations between 10,000 and with within tests Kinship correlation Mantel positive (6) used a We present, between is expected. differences structure is genetic nucleotide autocorrela- ecodist distances spatial of package spatial a spatial number to if and test, similar the haplotype this test For correlating between a distances. distances, conducted spatial haplotype we with m. mtDNA haplotypes females, 3200 using in to density structure analysis 215 kernel genetic tion from fixed spatial varied 95% evaluate distances the further These using To (ESRI). estimated 10.6 ranges Desktop home ArcGIS of with centroids between method distances used we distances, Peakall and r Smouse of and method Smouse the following analysis coefficient autocorrelation spatial correlation a conducted above) we see Peakall structure, locus, genetic by spatial t-test. (homozygosity evaluate paired To estimator a HL using using sexes calculated between was compared Coancestry heterozygosity and in Individual samples bootstrapping males. 1000 12 using compared then and r 1.0.1.9 estimator Wang’s using calculated was sbudbten- n n a eno eowe hr sn orlto.A esr fspatial of measure a As correlation. no is there when zero of mean a has and 1 and -1 between bound is 2–3 (2013). 526–530 , 75 91 16 (2000). 21–64 , 92 nti nlss swl si h et ecie eo,w nldd1 ape dl eae and females adult sampled 12 included we below, described tests the in as well as analysis, this In . 274 nPpeRpr 2.2.2 PopGenReport in rc al cd c.U .A. S. U. Sci. Acad. Natl. Proc. 1–4(2007). 219–24 , > 93 rnsEo.Evol. Ecol. Trends .8 ma o iuae aetosrn yd) eoddge isi dassharing (dyads kinship Second-degree dyads). parent-offspring simulated for r (mean 0.487 . . ta.Mlil yohssepanvraini xr-arptriya ieetlvl in levels different at paternity extra-pair in variation explain hypotheses Multiple al. et oeua Ecology Molecular r ewe ariegntcdsacs acltduigmcoaelt eoye with genotypes microsatellite using calculated distances, genetic pairwise between 92 79 ea.Ecol. Behav. n ariesaildsacs o ahdsac ls.Tecoefficient The class. distance each for distances, spatial pairwise and , eaaeyfrautfmlsadmls h nlsscluae the calculated analysis The males. and females adult for separately , 13 26 25 (1998). 52–58 , (2017). , 110 r ausadpdge eosrcini ooy First-degree Colony. in reconstruction pedigree and values 26 32–2(2013). 13328–32 , 5–6 (2015). 959–968 , 13 cec 8- ). (80-. Science eulslcinadtedseto man of descent the and selection Sexual rc .Sc il Sci. Biol. B Soc. R. Proc. 318 8218 (2007). 1882–1885 , cec 8- ). (80-. Science > .4 (mean 0.247 281 Proc. 1–8 , Biol. Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. 9 oln .P adnl,D .Dsesladetatrioilpopcigb slender-tailed by prospecting ( monkeys extra-territorial owl and monogamous in Dispersal dispersal W. Natal E. D. Fernandez-Duque, Chaco. Macdonald, & and mammals. P. Kalahari. choice in 30. S. south-western dispersal mate the Doolan, male in MHC, juvenile suricatta) G. predominant (Suricata meerkats and Cowlishaw, mates & for M. Competition 29. Raymond, F. S. J., Dobson, Wang, A., Behav. L. Knapp, primate. 28. E., social wild Huchard, a mammals. in and advantage birds heterozygote in dispersal and philopatry 27. systems, Mating J. P. Greenwood, (1980). 1140–1162 26. E. A. Leedale, Sci. Acad. Natl. 25. B. Hansson, Ecol. 24. W. Y. rodent. Sin, monogamous 24 a in tits choice mate blue 23. and in complex histocompatibility mating Major assortative S. Sommer, Heterozygosity-based Sociobiol. J. J. Sanz, 22. males & for J. choice active Ortego, show (2009). Garc´ıa-Navas, V., seals 2940 genetic fur Female individual W. and Amos, ( & production N. Egg P. Trathan, M. 21. J., J. Forcada, unrelated. Aparicio, I., and J. & heterozygous Hoffman, J. are P. that Cordero, inbred G., against Calabuig, 20. selection J., Parasite-mediated genetic Ortego, kestrels. J. against lesser Pemberton, defences in & post-copulatory diversity J. II: Smith, population. polyandry J., island 19. of Pilkington, living evolution free- D., The a Coltman, in W. sheep D. soay Zeh, & heterozygosity. A. 18. on J. based Zeh, choice mate of theory theory.incompatibility. A heterozygosity L. the J. of 17. Brown, review a the quality: genetic and and strategies 16. choice mating Mate MHC-associated B. dominant S. Kempenaers, Sommer, in & Behav. strategies primate. K. pair-living Mating Dausmann, obligate H. an J., 15. T. in Fietz, diversity Clutton-Brock, N., genetic Schwensow, & overall P. of mates. importance pair S. between Sharp, relatedness F., genetic 14. J. to relation Nielsen, in S., paternity Leclaire, extra-pair Biol. for offspring evidence increase meerkats: Females B. Kempenaers, 13. & T. A. marmots. J. Cohas, alpine Lifjeld, in paternity A., Johnsen, K., Delhey, 12. matings. K., extra-pair Foerster, through fitness and heterozygosity 11. ynse caeruleus Cyanistes 1835 (2015). 3138–3150 , 18 26 30 Behaviour 37 5–6 (2007). 157–164 , 4910 (2013). 1499–1507 , 1319 (1982). 1183–1192 , 58 8–7 (2007). 189–278 , 8–8 (2005). 181–189 , rc .Sc il Sci. Biol. B Soc. R. Proc. 0982 22) doi:10.1073/pnas.1918726117 (2020). 201918726 tal. et tal. et 146 tal. et :ipiain o h vlto fmt choice. mate of evolution the for implications ): tal. et 8–0 (2009). 583–606 , H ls Iasraiemt hiei uoenbdes( badgers European in choice mate II-assortative class MHC h eei iiaiybtenpi ebr nune h rqec fextrapair of frequency the influences members pair between similarity genetic The oeiec o nreigaodnei ra edwrlrpopulation. warbler reed great a in avoidance inbreeding for evidence No o.Ecol. Mol. ot ik n viac fibedn nacoeaieybedn bird. breeding cooperatively a in inbreeding of avoidance and risk, Cost, nm Behav. Anim. Nature 16 3329 (2007). 2383–2392 , 264 76 445 vlto N Y). (N. Evolution 79 (2008). 87–95 , 97 (1997). 69–75 , o.Ecol. Mol. 1–1 (2007). 912–914 , 14 Nature 19 .Zool. J. 5526 (2010). 2545–2561 , 425 53 1–1 (2003). 714–717 , 2916 (1999). 1259–1267 , rc .Sc il Sci. Biol. B Soc. R. Proc. 240 ea.Ecol. Behav. 97 (1996). 59–73 , vl Ecol. Evol. ou azarai Aotus ee meles Meles 8 06 (1997). 60–65 , 22 fteArgentinean the of ) 1–3 (2008). 617–636 , nm Behav. Anim. ea.Ecol. Behav. ). d.Study Adv. 276 o.Ecol. Mol. .Evol. J. 2931– , Behav. Anim. Proc. 28 , Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. 7 oa,A,Yco,N . aSla . oses .&Ali´,D xr-arptriyi the in paternity Extra-pair Allain´e, D. & B. Goossens, A., Silva, Da G., N. Yoccoz, A., Sociobiol. Ecol. Cohas, ( marmot alpine monogamous 47. previous C. Barelli, on (2013). 1185–1195 replacements adult of 46. effects divorce: of S. P. Children Nimje, beavers. E. Fernandez-Duque, & a 45. in M. intrasexual-competition monkeys. Huck, part: owl us Argentinean do in intruder) their offspring an and (or birds, death Till 44. in M. dynamics Huck, and & E. strategies Fernandez-Duque, primate. Floater monogamous populations. M. avian M. in 43. Delgado, nonbreeders & of understanding M. an Ferrer, towards V., Conserv. biology: in Penteriani, conservation spacing and in size, importance range calls, loud Intergroup 42. G. J. relation- Robinson, Anthropol. & male–female Phys. G. monogamy, W. J. Social Kinzey, Am. E. Fernandez-Duque, ( & monkeys A. titi 41. wild Fiore, torquatus). in Di (Callicebus care monkey A., biparental titi Spence-Aizenberg, the and in ships, primate: behavior Neotropical Grooming a C. 40. P. in Wright, bond & pair G. a W. makes Kinzey, What Primatol. W. PCR- E. and Heymann, sampling 39. & DNA S. non-invasive Walker, contributions. by S., male Dolotovskaya, tested and parentage female gibbons’ Wild O. 38. Takenaka, & T. microsatellites. Oka, polymorphic 2013). amplified Press, University (Cambridge 295–302 37. A.) uacaris M. and equatorial Norconk, sakis in & parenting titis, and F. of relationships S. Pair-mate conservation G. and ( A. Luna, biology monkey de Evolutionary & titi Di ( A. the monkeys Fiore, E., saki in Fernandez-Duque, pairbond The 36. G. Anzenberger, pairmates. in the Callicebus). of (genus contributions 2013). monkeys titi Press, University of (Cambridge behavior 35. 196–207 and uacaris Ecology A.) and W. M. sakis E. Norconk, titis, Heymann, & of & F. conservation C. J. and Bicca-Marques, biology Evolutionary monkeys titi red wild of 34. history life and Demography A. Primatol. Fiore, J. Di Am. & E. Fernandez-Duque, mammal S., monogamous Belle, Van the ( in dispersal Female-biased 33. N. Perrin, & J. Goudet, (1997). F., rodent, 127–132 Balloux, monogamous L., Favre, russula a Crocidura in Dispersal O. 32. D. Ribble, (1992). 31. alcbsdiscolor Callicebus er Prepr. PeerJ 14 3 6–7 (1982). 267–275 , 3–4 (2011). 233–241 , ihcaaequatorialis Pithecia 59 tal. et 78 vdnefo eddt n irstliepatterns. microsatellite and data field from evidence : tal. et 9–0 (2006). 597–605 , n qaoilsks( sakis equatorial and ) 0–1 (2016). 204–215 , 7 LSOne PLoS lotfihu:SPmresrva o eeso xr-arptriyi h Eurasian the in paternity extra-pair of levels low reveal markers SNP faithful: Almost xr-arptriycnre nwl ht-addgibbons. white-handed wild in confirmed paternity Extra-pair 2861(2019). e27866v1 , 60 3–4 (1983). 539–544 , amt marmota Marmota .Sc pnSci. Open Soc. R. oi Primatol. Folia 8 574(2013). e53724 , n e iimnes( monkeys titi red and ) Primates ea.Eo.Sociobiol. Ecol. Behav. ihcaaequatorialis Pithecia 50 alcbsdiscolor Callicebus 42 :terlso oilstigadfml aechoice. mate female and setting social of roles the ): 7 8–0 (1988). 188–203 , 77 (2001). 67–73 , 949(2019). 191489 , 15 eoycscalifornicus Peromyscus < alcbsmoloch Callicebus 66 /i es eg,L . ant,A . Ferrari, A., A. Barnett, M., L. Veiga, (eds. nAaoinEudr 2ya study. 12-year a Ecuador: Amazonian in ) es ant,A,Via .M,Frai S. Ferrari, M., L. Veiga, A., Barnett, (eds. > 0–1 (2012). 505–517 , ). alcbsdiscolor Callicebus Primates rc .Sc il Sci. Biol. B Soc. R. Proc. 57 :itiscvru extrinsic versus intrinsic ): 0–1 (2016). 103–112 , . < m .Primatol. J. Am. Ecology alcbstorquatus Callicebus /i > fEudr in Ecuador. of ) 73 859–866 , m J. Am. Behav. Anim. 264 75 . , , Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. 4 ortr . ac,M,Jhsn .&Kmear,B pta eei tutr n ffcsof effects and structure genetic spatial A E. B. Geffen, Kempenaers, & behavioural (2011). A. population. and Johnsen, bird Genetic M., wild 65. G. Valcu, a Malarky, in K., choice & Foerster, mate E. on P. relatedness Komers, Reproductive M., kirkii). B. (Madoqua J. 64. Lasley, dik–dik Pemberton, & Kirk’s M., A. mammal, N. a W. P. 264 in Mason, Brotherton, monogamy E., of Fernandez-Duque, evidence P., S. Mendoza, 63. R., ( monkeys C. titi Valeggia, female of monkey wild titi biology the in of breeding paternity on 62. Notes of A. Klaiber-Schuh, Patterns & A. C. Welker, B., Primatol. Fiore, Jantschke, Folia Di & 61. E. Fernandez-Duque, of A., in density Martins, abstract). population Primatologists S., (conference Estimating A. Belle, Ecuador Fiore, Van Station, Di ( & titis monogamous E. socially Fernandez-Duque, G., A. Luna, 60. De tamarins. A., ( and Dacier, monkeys sakis, titi cooperative Amazonian monkeys, and titi monogamy, sexual monkeys, pair-living, 59. owl of wild evolution The on Di. research A. from Fiore, Anthropol. & insights E. care: Fernandez-Duque, 2013). (genus infant Press, monkeys University titi (Cambridge of 196–207 behavior 58. A.) and uacaris Ecology M. and W. Norconk, sakis E. & titis, Heymann, F. & of S. conservation C. monkey, J. and American Bicca-Marques, biology South Evolutionary the of organization 57. Social A. comparative W. a Mason, birds: report. in fertilizations extra-pair 56. and Density W. Syr˚uˇckov´a, ( P. beaver Sherman, birds. & in A. F. 55. copulations D. extra-pair Westneat, of evolution birds? and analysis. in ecology promiscuity The of 54. F. cost D. possible Westneat, a conflict. diseases: (1990). and transmitted 331–369 correlates, Sexually causes, C. birds: Wilks, 53. in & paternity A. Extra-pair Poiani, K. R. 117 I. Stewart, & within 52. males F. Syst. new D. and Evol. Westneat, old Ecol. of Rev. relations Annu. familial stepfathers: and Fathers J. 51. ( F. Bossuyt, monkeys & titi S. P. brown of Rodman, in groups bond gibbons pair golden-cheeked the in 50. Understanding paternity thesis). J. Extrapair (PhD Lawrence, interests D. reprodcutive Chivers, female & T. V. 49. Binh, C., Roos, M., 82 Kenyon, ( 48. oacsgabriellae Nomascus 5–6 (2011). 154–164 , 7–8 (1997). 675–681 , (2000). 1061–1065 , uaeSu Zool Stud Tulane atrfiber Castor ea.Eo.Sociobiol. Ecol. Behav. alcbsbrunneus Callicebus –6(00.doi:10.1111/j.1365-2958.2003.03935.x (2020). 1–86 (2016). 65 tal. et 1–1 (1995). 210–213 , ). ntescnaylwadfrs fCtTe ainlPr,Vietnam. Park, National Tien Cat of forest lowland secondary the in ) tal. et amlRes. Mammal i none aeadibedn viac ncanids. in avoidance inbreeding and rate encounter Kin 13 alcbsdiscolor Callicebus alcbsdiscolor Callicebus eei eainhp ihnclne ugs eei ooayi h Eurasian the in monogamy genetic suggest colonies within relationships Genetic 32 (1966). 23–28 , 34 nsuhatr eu[Abstract]. Peru southeastern in alcbsmoloch Callicebus 6–9 (2003). 365–396 , 41 0–1 (1997). 205–215 , 60 3–4 (2015). 139–147 , h Thesis PhD nentoa rmtlgclSceyadAeia oit of Society American and Society Primatological International i lyakpitcounts. point playback via ) n ai ( sakis and ) ncaptivity. in ) 16 o.Ecol. Mol. Clmi nvriy e ok 2007). York, New University, (Columbia ihcaaequatorialis Pithecia mJPy Anthr. Phys J Am m .Primatol. J. Am. es eg,L . ant,A . Ferrari, A., A. Barnett, M., L. Veiga, (eds. 15 5546 (2006). 4555–4567 , rc .Sc odnBBo.Sci. Biol. B London Soc. R. Proc. Biotropica alcbsmoloch Callicebus alcbsbrunneus Callicebus tteTptn Biodiversity Tiputini the at ) o.Ecol. Mol. 47 132 8–9 (1999). 183–195 , 43 0 (2007). 201 , 3–4 (2011). 135–140 , alcbscupreus Callicebus ur Ornithol. Curr. oi Primatol. Folia preliminary a : 20 Callicebus er.Phys. Yearb. 5348–5358 , :ml and male ): .in ). Auk 7 . , Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. 4 oe,O .&Wn,J OOY rga o aetg n isi neec rmmultilocus from inference sibship and parentage for program a COLONY: J. Wang, & R. markers. O. molecular Jones, using data. genotype relatedness pairwise for estimator 84. relatedness An pairwise analysing J. for Wang, CERVUS package R program an (2002). computer related: R. the T. Frasier, how & 83. Revising J. Wang, C. H., markers. P. T. molecular Muir, Marshall, J., codominant Pew, & from L. M. for assignment. interface Taper, paternity 82. user T., in graphical success S. multiplatform increases Kalinowski, a error 4: genotyping version accommodates R. view in Sea O. analyses Gascuel, 81. genetic building. & population tree S. phylogenetic basic Guindon, and M., simplifying Gouy, alignment PopGenReport: sequence B. Gruber, & 80. software T. MICRO-CHECKER: P. A. Shipley, Adamack, Evol. & Ecol. M. P. Methods D. data. Wills, microsatellite F., in 79. W. primates. errors Hutchinson, genotyping non-human C., correcting in Oosterhout, assignment and Van identifying sex for for method genetic rapid 78. A A. Fiore, Di (2005). 1053–1058 diversity chimpanzees. J. 77. Genetic wild C. H. in P. diversity Barbian, M. allelic Schneider, greater reveals & F. S. Ferrari, 76. A., Silva, C., Gon¸calves, E. A., mating ( Genet. L. on titis Menescal, studies red-bellied for of suitable loci microsatellite 75. of ( evaluation monkeys and titi Characterization red in B. aequatorialis identity A. genetic Martins, and parentage, system, 74. sync? I should or store, A. I Mendoza, availability.captive Should resource B. M. predictable Nagy-Reis, under 73. anti- & primates Active C. C. Neotropical W. Gestich, small E. B., two Heymann, C. 60 of & parental Caselli, P., F. strategy of J. Nummert, breeding costs Souza-Alves, E., The with C. cope cupreus). Haas, to (Plecturocebus C., 72. strategies monkeys Amasifuen, more: titi Flores eat red S., of or Dolotovskaya, behaviour less predator Do population. W. bird E. wild 71. Heymann, a in & monkey. avoidance pair-living S. inbreeding Dolotovskaya, a of in means care a as Dispersal C. 70. Sci. B. Sheldon, Biol. & B M. Soc. Szulkin, R. Proc. 69. structure social of sifaka. consequences of golden-crowned Genetic Qu´em´er´e, species L. the B., Chikhi, Parreira, in some & I. construction. Why Vanp´e, Carvalho, network P. E., C., haplotype for D. 68. software Full-feature POPART: Armstrong, D. Bryant, & & H. W. Evol. J. Kokko, Leigh, Ecol. N., L. Tracy, saddlebacks. 67. and S., robins S. Zealand Taylor, New from G., Insights I. (2009). inbreeding: avoid Jamieson, not do birds 66. 1–1 (2019). 113–118 , 47 alcbscupreus Callicebus 3–4 (2009). 235–240 , 6 .(h nvriyo ea tAsi,2015). Austin, at Texas of University (The ). 1011 (2015). 1110–1116 , o.Eo.Resour. Ecol. Mol. tal. et alcbsmoloch Callicebus 5 8–8 (2014). 384–387 , tal. et ouaingntc fteClfri ainlPiaeRsac etrs(CNPRC) Center’s Research Primate National California the of genetics Population 275 colony. nm Behav. Anim. eeiy(Edinb). Heredity HIP natmtdhg-hogptmcoaelt eoyigplatform genotyping microsatellite high-throughput automated an CHIIMP: 0–1 (2008). 703–711 , Primates 10 o.Eo.Resour. Ecol. Mol. 5–5 (2010). 551–555 , rmEsenAaoi ae nmcoaelt markers. microsatellite on based Amazonia Eastern from ) 163 56 74 (2015). 37–44 , 6–7 (2020). 163–173 , –2(00.doi:10.1038/s41437-020-0345-5 (2020). 1–12 o.Bo.Evol. Biol. Mol. cl Evol. Ecol. 17 15 5–6 (2015). 557–561 , alcbsdiscolor Callicebus 16 rmt Biol. Primate 9676 (2018). 7946–7963 , 27 o.Eo.Notes Ecol. Mol. 2–2 (2010). 221–224 , o.Ecol. Mol. n aimnes( monkeys saki and ) 6 96 (2019). 59–64 , Genetics ea.Ecol. Behav. 16 0910 (2007). 1099–1106 , osr.Genet. Conserv. 4 3–3 (2004). 535–538 , 160 20 1203–1215 , 575–584 , Biochem. Primates Methods Pithecia 6 , Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. h eerhwsfne yGra rmt etr ekyFudto,Gra eerhFoundation Fund. Research Action German Primate Foundation, and Leakey Society Primatological Center, International Primate 407493972), German nr. Center. by Project Primate funded (DFG; German was the and research Fauna Agriculture) de The of y Forestal authorities Ministry relevant Nacional Peruvian the Servicio the from the guidelines from of We 249-2017-SERFOR/DGGSPFFS ethical Silvestre no. possible. and permit permissions been laboratory. (research necessary have Peru genetics all of not the under would conducted in work was work work field excellent This the her whom for Mar´echal, without Schwarz Mathieu assistants Christiane Tello, field thank Shahuano other also Ney all Arirama, and Huanuiri Walker, Amasifu´en,Sarah Migdonio Flores Camilo vole thank Taiwan We the in system Monogamous Acknowledgments K. L. Lin, & 81 J. G. Bonadonna, P. Chiang, ranges. 100. S., home and J. DNA Wu, microsatellite from inferred paternity and 99. polymorphism II class (MHC) complex histocompatibility (1999). of Major 1259–1272 H. Tichy, system monogamous & mating S. the Sommer, in monogamous The O. 98. D. Ribble, monogamy for evidence genetic fingerprinting. and bonding pair Long-term D. 97. S. Gehrt, complexity. & ( social J. coyotes Dubach, studying A., urban ‘monogamy’ for C. Hennessy, among of framework evolution A The M. oranges? P. 96. and Kappeler, apples Of data. E. Fernandez-Duque, ecological & of 95. A. analysis Fiore, dissimilarity-based Di for M., package primates. Huck, non-human ecodist in The L. D. Urban, multilocus 94. & and C. multiallele S. individual Softw. Goslee, of Stat. analysis J. autocorrelation Spatial R. Peakall, 93. & inbreeding E. and P. relatedness Smouse, structure. analysing genetic and estimating simulating, for 92. program a Coancestry: J. Wang, coefficients. 91. A. Alexander, macrocephalus heterozygosity. pairwise individual estimate microsatellite-based to 90. of function R comparison easy-to-use A an Genhet: E. A. Matthysen, Coulon, 10 & P. Galbusera, 89. T., markers. Casteele, molecular de with Van relatedness estimators. pairwise relatedness of Estimation K. 88. Ritland, & relatedness. M. and chance Lynch, to (1999). due 1753–1766 fingerprints DNA of Similarity A. 87. Chakravarti, & E. D. Weeks, patterns. C., mating Hered. C. and Li, Hum. relatedness of hypotheses testing 86. for software STORM: R. T. Frasier, Resour. 85. 293(2019). e22993 , (2010). 167–169 , 8 2316 (2008). 1263–1266 , o.Eo.Resour. Ecol. Mol. 43 )? ea.Eo.Sociobiol. Ecol. Behav. 22 55 (1993). 45–52 , o.Ecol. Mol. –9(2007). 1–19 , eeiy(Edinb). Heredity yoemsantimena Hypogeomys tal. et ai latrans Canis tal. et o.Ecol. Mol. rn.Eo.Evol. Ecol. Front. vdneo eei ooayi h eu nr ( Indri lemur the in monogamy genetic of Evidence 25 htiflecstewrdiegntcsrcueo pr hls( whales sperm of structure genetic worldwide the influences What 7427 (2016). 2754–2772 , 11 4–4 (2011). 141–145 , 10 ). 82 5914 (2001). 1539–1549 , 29 .Mammal. J. 6–7 (1999). 561–573 , 6–6 (1991). 161–166 , h nagrd ags nei aaayrodent. Malagasy endemic largest endangered, the , 7 7 (2020). 472 , 93 ol Stud. Zool. 18 3–4 (2012). 732–742 , eoycscalifornicus Peromyscus 51 0–1 (2012). 204–212 , ea.Eo.Sociobiol. Ecol. Behav. nr indri Indri srvae yDNA by revealed as ). o.Eo.Resour. Ecol. Mol. irtskikuchii Microtus m .Primatol. J. Am. 73 Genetics o.Ecol. Mol. 3(2019). 13 , o.Ecol. Mol. Physeter 152 8 , , Posted on Authorea 28 Aug 2020 — The copyright holder is the author/funder. All rights reserved. No reuse without permission. — https://doi.org/10.22541/au.159492953.34696224/v2 — This a preprint and has not been peer reviewed. Data may be preliminary. pce apesize Sample ( gibbons White-handed ( gibbons Golden-cheeked ( Indri ( beaver Eurasian ( vole ( Taiwan rat jumping giant Malagasy ( mouse California ( Coyotes ( dik-dik Kirk’s ( gibbon Bornean ( monkey Also owl Azara’s detected. (EPP) paternities rate extra-pair EPP Species no the with with mammals species monogamous monogamous genetically genetically predominantly two of included List 2. Table care. than offspring more births provide over multiple and regularly litter of births) per set singleton infant care a with one Biparental over than species other more for each produce seasons that with reproductive species exclusively consecutive for offspring one season produce reproductive one female least adult (at one season. and reproductive male one adult least at monogamy during relationship Genetic mating exclusive an have female adult emotional, behavioral, by monogamy evidenced Sexual as adults, other of characteristics. exclusion the endocrinological to and relationship affiliative “social an as have to female referred often is This Pair-bonded offspring. non-reproducing their with possible monogamy”. range, home a based share and female 2020) Fernandez-Duque, & 2019). Fiore, Pair-living (Kappeler, Di (Huck, Kappeler in of proposed framework study, the this on in Center. used Terminology Primate German 1. Table the and Peru of of Ministry Peruvian authorities relevant the Tables the of Silvestre from Fauna guidelines de ethical y and Forestal Nacional Agriculture) Servicio the from SERFOR/DGGSPFFS to related data Ethics Additional ([email protected]). C.R. Materials. or Supplementary ([email protected]) Interests the S.D. Competing from and/or requested paper be the may in paper present this are animals, study Accessibility: Data analysed E.W.H. and and work C.R. laboratory did S.D., information field, by the Additional written in was data paper collected S.D. The study. data. the the designed E.W.H. and C.R. S.D., contributions Author nr indri Indri hswr a odce ne l eesr emt rsac emtn.249-2017- no. permit (research permits necessary all under conducted was work This : ai latrans Canis wolvswt whom) with lives (who irtskikuchii Microtus woi ffiitdwt hm:atp fsca tutr hr n dl aeadoeadult one and male adult one where structure social of type a whom): with affiliated is (who aou kirkii Madoqua 2osrn f7fml rus(6aiasi total) in animals (26 groups family 7 of offspring 12 ) yoae muelleri Hylobates atrfiber Castor eoycscalifornicus Peromyscus wopoie aetlcr) yeo aesse hr ohradpttv father putative and mother a where system care of type a care): parental provides (who womtswt hm:atp fsca aigsse hr n dl aeadone and male adult one where system mating social of type a whom): with mates (who ou azarae Aotus l aanee oeaut h ocuin nteppr nldn eoye fall of genotypes including paper, the in conclusions the evaluate to needed data All 6osrn f1 aiygop 26aiasi total) in animals (236 groups family 18 if offspring 96 ) wopoue ffpigwt hm:atp fgntcmtn ytmweeone where system mating genetic of type a whom): with offspring produces (who h uhr elr ocmeiginterests. competing no declare authors The : yoae lar Hylobates oacsgabriellae Nomascus yoemsantimena Hypogeomys a 8osrn f9clne ls6fml ruswt nyaut 3 nml nttl Sruco´ ta. 05;()16osrn f4 aiygop 36aiasi oa)()1 irstlielc;()2 igencetd polymorphisms nucleotide single 27 (b) loci; microsatellite 15 (a) total) in animals (356 groups family 48 of offspring (Syr˚uˇckov´a 166 total) (b) in 2015); animals al., (38 et adults only with groups family 6 plus colonies 9 of offspring 18 (a) ) 2osrn f1 aiygop 6 nml ntotal) in animals (68 groups family 11 of offspring 12 ) 1osrn f2 aiygroups family 20 of offspring 31 ) 5osrn f2 aiygop 18aiasi total) in animals (128 groups family 29 of offspring 35 ) ffpigo aiygop 1 nml ntotal) in animals (13 groups family 4 of offspring 4 ) : 1osrn,2 oni arlvn rusad1 oni ut-aegop 8 nml ntotal) in animals (89 groups multi-male in born 15 and groups pair-living in born 27 offspring, 41 ) yeo oilognzto hr n dl aeadoeadult one and male adult one where organization social of type a 2osrn f2 opeegop,pu 7osrn rmicmlt rus(ape rmfte rmte o vial)DAfigrrniguigrsrcinenzyme restriction using fingerprinting DNA available) not mother or father from (samples groups incomplete from offspring 17 plus groups, complete 22 of offspring 82 ) 0osrn f6fml rus(9aiasi total) in animals (29 groups family 6 of offspring 10 ) 0osrn f2 aiygop 19aiasi total) in animals (139 groups family 28 of offspring 60 ) 19 < 0.1. oyopim famjrhsooptblt ope ls Ign Q sn eunigadsnl-tadcnomto oyopimaayi ,wt ae fml n ae ffml elcmn u oltessrdb utpefathers multiple by sired litters no but replacement female of cases 3 and male of cases 3 with 0, analysis polymorphism conformation single-strand and sequencing using DQA gene II class complex histocompatibility major a of Polymorphisms 2mcoaelt loci microsatellite 12 loci microsatellite 8 loci microsatellite 6 0mcoaelt loci microsatellite 10 loci microsatellite 12 loci microsatellite 7 loci microsatellite 14 used method Genotyping 6mcoaelt loci microsatellite 16 a ,wt n osbefml elcmn u oltessrdb utpeftes b ,crepnigt h P rprino .5;7osrn eesrdb egbrn ae,i ae h aent ol o easge a Sruco´ ta. 05;()(ij ta. 2019) al., et (Syr˚uˇckov´a (Nimje (a) (b) 2015); al., et assigned be not could paternity the assigned cases be 2 not in could males, paternity neighboring the by case sired 1 were in father offspring likely males, 7 as neighboring father 0.054; by indicated genetic of sired male as were proportion other confirmed 2 EPP no male 0.073; the but non-territorial of to father lone proportion genetic corresponding a EPP as 9, 0.1; the excluded (b) of to father fathers; proportion multiple corresponding social EPP by 3, 0.083; the sired of to fathers litters proportion multiple corresponding no EPP by 1, but the sired replacement to litters female corresponding no possible 1, but one replacement with female 0, of (a) cases 2 with 0, 0 0 0 0 found cases EPP of N 0 Brlie l,2013) al., et (Barelli 2011) al., et (Kenyon 2019) al., et (Bonadonna 2012) Lin, & Chiang, (Wu, 1999) Tichy & (Sommer 1991) 2012) (Ribble, Gehrt, & Dubach, (Hennessy, 1997) al., et (Brotherton 2001) Takenaka, & (Oka 2014) al., et (Huck References