Kin-biased spatial associations and social interactions in male and female black howler monkeys (Alouatta pigra)

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Kinship has been shown to play a crucial role in shaping the social structure of animal societies. We examined the genetic relationships of adult and sub-adult males (N=17) and females (N=15) from five social groups of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico, by genotyping each individual at 21 microsatellite markers. These findings were related to patterns of intragroup spatial associations and affiliative and agonistic interactions recorded over a 28-month period of behavioural observation in the field. We demonstrate that the social structure of this black howler monkey population is dominated by strong social relationships and high degrees of genetic relatedness among females. Female kin had stronger relationships because they were less aggressive to each other than female non-kin. Nevertheless, females resident in the same social group frequently spent time close to one another and affiliated with each other regardless of kinship. Relationships among males from the same social group were based on avoidance and tolerance, as males rarely interacted either affiliatively or agonistically and spent limited time close to one another. Nonetheless, kinship was a significant predictor of agonistic interactions among males, with unrelated or distantly related males engaging in agonism at higher rates than close male kin. Adult males and females rarely co-resided with adult kin from the opposite sex, and they affiliated and spatially associated at rates intermediary to those among females and those among males.

Kin-biased spatial associations and social interactions in male and female black howler monkeys (Alouatta pigra)

in Behaviour

Sections

References

AltmannJ. (1974). Observational study of behavior: sampling methods. — Behaviour 69: 227-267.

ArchieE.A.MaldonadoJ.E.Hollister-SmithJ.A.PooleJ.H.MossC.J.FleischerR.C.AlbertsS.C. (2008). Fine-scale population genetic structure in a fission–fusion society. — Mol. Ecol. 17: 2666-2679.

AvilésL.AbbotP.CutterA.D. (2002). Population ecology, nonlinear dynamics, and social evolution. I. Associations among nonrelatives. — Am. Nat. 159: 115-127.

BöhleU.R.ZischlerH. (2002). Polymorphic microsatellite loci for the mustached tamarin (Saguinus mystax) and their cross-species amplification in other New World monkeys. — Mol. Ecol. Notes 2: 1-3.

BorgattiS.P.EverettM.G.FreemanL.C. (2002). Ucinet 6 for Windows: software for social network analysis. — Analytic TechnologiesHarvard, Cambridge, MA.

BrockettR.C.HorwichR.H.JonesC.B. (2000). Female dispersal in the Belizean black howling monkey Alouatta pigra. — Neotrop. Primates 8: 32-34.

Calegaro-MarquesC.Bicca-MarquesJ.C. (1996). Emigration in a black howling monkey group. — Int. J. Primatol. 17: 229-237.

CameronE.Z.SetsaasT.H.LinklaterW.L. (2009). Social bonds between unrelated females increase reproductive success in feral horses. — Proc. Natl. Acad. Sci. USA 106: 13850-13853.

ChapaisB. (2006). Kinship, competence, and cooperation in primates. — In: Cooperation in primates and humans: mechanisms and evolutions ( KappelerP.M.van SchaikC.P. eds). SpringerNew York, NY p.  47-63.

ChapaisB.BermanC.M. (eds) (2004). Kinship and behavior in primates. — Oxford University PressNew York, NY.

ClarkeM.R.GlanderK.E. (2008). Natal emigration by both sexes in the La Pacifica population of mantled howlers: when do some stay?Am. J. Primatol. 70: 195-200.

Clutton-BrockT. (2009). Cooperation between non-kin in animal societies. — Nature 462: 51-57.

CollevattiR.G.Souza-NetoA.C.Silva-JrN.J.TellesM.P.C. (2013). Kin structure and parallel dispersal in the black-and-gold howler monkey Alouatta caraya (Platyrrhini, Atelidae). — Genet. Mol. Res. 12: 6018-6031.

Cortés-OrtizL.MondragónE.CabotajeJ. (2010). Isolation and characterization of microsatellite loci for the study of Mexican howler monkeys, their natural hybrids, and other Neotropical primates. — Conserv. Genet. Resourc. 2: 21-26.

CrockettC.M. (1984). Emigration by female red howler monkeys and the case for female competition. — In: Female primates: studies by women primatologists ( SmallM.F. ed.). AR LissNew York, NY p.  159-173.

CrockettC.M.JansonC.H. (2000). Infanticide in red howlers: female group size, male membership, and a possible link to folivory. — In: Infanticide by males and its implications ( van SchaikC.P.JansonC.H. eds). Cambridge University PressCambridge p.  75-98.

CrockettC.M.PopeT.R. (1993). Consequences of sex differences in dispersal for juvenile red howler monkeys. — In: Juvenile primates: life history development and behavior ( PereiraM.E.FairbanksL.A. eds). Oxford University PressOxford p.  104-118.

DekkerD.KrackhardtD.SnijdersT.A.B. (2007). Sensitivity of MRQAP tests to collinearity and autocorrelation conditions. — Psychometrika 72: 563-581.

Di FioreA. (2012). Genetic consequences of primate social organization. — In: The evolution of primate societies ( MitaniJ.C.CallJ.KappelerP.M.PalombitR.A.SilkJ.B. eds). University of Chicago PressChicago, IL p.  269-292.

Di FioreA.FleischerR.C. (2005). Social behavior, reproductive strategies, and population genetic structure of Lagothrix poeppigii. — Int. J. Primatol. 26: 1137-1173.

DiasP.A.D.Rodriguez-LunaE.Canales-EspinosaD. (2008). The function of the “greeting ceremony” among male mantled howlers (Alouatta palliata) on Agaltepec Island, Mexico. — Am. J. Primatol. 70: 1-8.

DiasP.A.D.Rangel-NegrínA.VeàJ.J.Canales-EspinosaD. (2010). Coalitions and male–male behavior in Alouatta palliata. — Primates 51: 91-94.

Díaz GallegosJ.R. (1996). Estructura y composición florística de la vegetación del Parque Nacional Zona Arqueológica de Palenque Chiapas México. — Bs. thesis Universidad Juárez Autónoma de Tabasco Mexico.

EllsworthJ.A.HoelzerG.A. (1998). Characterization of microsatellite loci in a New World primate, the mantled howler monkey (Alouatta palliata). — Mol. Ecol. 7: 657-658.

EstradaA.CastellanosL.IbarraA.Garcia del ValleY.MuñozD.RiveraA.FrancoB.FuentesE.JiménezC. (2002). Survey of the population of the black howler monkey, Alouatta pigra, at the Mayan site of Palenque, Chiapas, Mexico. — Primates 44: 51-58.

FrèreC.H.KrützenM.MannJ.Watson-CappsJ.J.TsaiY.J.PattersonE.M.ConnorR.BejderL.SherwimW.B. (2010). Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins. — Anim. Behav. 80: 481-486.

GarrowayC.J.BowmanJ.WilsonP.J. (2013). Complex social structure of southern flying squirrels is related to spatial proximity but not kinship. — Behav. Ecol. Sociobiol. 67: 113-122.

GeroS.EngelhauptD.WhiteheadH. (2008). Heterogeneous social associations within a sperm whale, Physeter macrocephalus, unit reflect pairwise relatedness. — Behav. Ecol. Sociobiol. 63: 143-151.

GilbyI.C. (2012). Cooperation among non-kin: reciprocity, markets, and mutualism. — In: The evolution of primate societies ( MitaniJ.C.CallJ.KappelerP.M.PalombitR.A.SilkJ.B. eds). University of Chicago PressChicago, IL p.  514-530.

GlanderK.E. (1980). Reproduction and population growth in free-ranging mantled howling monkeys. — Am. J. Phys. Anthropol. 53: 25-36.

GlanderK.E. (1992). Dispersal patterns in Costa Rican mantled howling monkeys. — Int. J. Primatol. 13: 415-436.

GonçalvesE.C.SilvaA.BarbosaM.S.R.SchneiderM.P.C. (2004). Isolation and characterization of microsatellite loci in Amazonian red-handed howlers Alouatta belzebul (Primates, Platyrrhini). — Mol. Ecol. Notes 4: 406-408.

GrativolA.D.BallouJ.D.FleischerR.C. (2001). Microsatellite variation within and among recently fragmented populations of the golden lion tamarin (Leontopithecus rosalia). — Conserv. Genet. 2: 1-9.

GrinnellJ.PackerC.PuseyA.E. (1995). Cooperation in male lions: kinship, reciprocity or mutualism?Anim. Behav. 49: 95-105.

HamiltonW.D. (1964). The genetical evolution of social behavior I and II. — J. Theor. Biol. 7: 1-52.

HindeR.A. (1976). Interactions, relationships and social structure. — Man 11: 1-17.

HirschB.T.StantonM.A.MaldonadoJ.E. (2012). Kinship shapes affiliative social networks but not aggression in ring-tailed coatis. — PLoS ONE 7: e37301.

HirschB.T.PrangeS.HauverS.A.GehrtS.D. (2013). Genetic relatedness does not predict racoon social network structure. — Anim. Behav. 85: 463-470.

HoL.Cortés-OrtizL.DiasP.A.D.Canales-EspinosaD.KitchenD.BergmanT.J. (2014). Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids. — Am. J. Primatol. DOI:10.1002/ajp.22273.

HoezlerG.A.MoralesJ.C.MelnickD.J. (2004). Dispersal and the population genetics of primate species. — In: Kinship and behavior in primates ( ChapaisB.BermanC.M. eds). Oxford University PressNew York, NY p.  109-131.

HorwichR.H.BrockettR.C.JonesC.B. (2000). Alternative male reproductive behaviors in the Belizean black howler monkey (Alouatta pigra). — Neotrop. Primates 8: 95-98.

HothornT.HornikK.van de WielM.A.ZeileisA. (2008). Implementing a class of permutation tests: the coin package. — J. Stat. Software 28: 1-23.

JackK.M.FediganL.M. (2004). Male dispersal patterns in white-faced capuchins, Cebus capucinus. Part 2: patterns and causes of secondary dispersal. — Anim. Behav. 67: 771-782.

JonesC.B. (1980). The function of status in the mantled howler monkey, Alouatta palliata Gray: intraspecific competition for group membership in a Neotropical folivorous primate. — Primates 21: 389-405.

KalinowskiS.T.TaperM.L.MarshallT.C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. — Mol. Ecol. 16: 1099-1106.

KapsalisE. (2004). Matrilineal kinship and primate behavior. — In: Kinship and behavior in primates ( ChapaisB.BermanC.M. eds). Oxford University PressNew York, NY p.  153-176.

KitchenD.M.HorwichR.H.JamesR.A. (2004). Subordinate male black howler monkey (Alouatta pigra) responses to loud calls: experimental evidence for the effects of intra-group male relationships and age. — Behaviour 141: 703-723.

KonovalovD.A.ManningC.HenshawM.T. (2004). KINGROUP: a program for pedigree relationships reconstruction and kin group assignments using genetic markers. — Mol. Ecol. Notes 4: 779-782.

KrackhardtD. (1987). QAP partialling as a test of spuriousness. — Soc. Networks 9: 171-186.

KrackhardtD. (1988). Predicting with networks. Nonparametric multiple-regression analysis of dyadic data. — Soc. Networks 10: 359-381.

LangergraberK.E.MitaniJ.C.VigilantL. (2007). The limited impact of kinship on cooperation in wild chimpanzees. — Proc. Natl. Acad. Sci. 104: 7786-7790.

LangergraberK.E. (2012). Cooperation among kin. — In: The evolution of primate societies ( MitaniJ.C.CallJ.KappelerP.M.PalombitR.A.SilkJ.B. eds). University of Chicago PressChicago, IL p.  491-513.

Lawson HandleyL.J.PerrinN. (2007). Advances in our understanding of mammalian sex-biased dispersal. — Mol. Ecol. 16: 1559-1578.

ManlyB.F.J. (2007). Randomization bootstrap and Monte Carlo methods in biology3rd edn.Chapman & HallLondon.

MartinsW.P.StrierK.B. (2004). Age at first reproduction in philopatric female muriquis (Brachyteles arachnoides hypoxanthus). — Primates 45: 63-67.

MiltonK.LozierJ.D.LaceyE.A. (2009). Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. — Conserv. Genet. 10: 347-358.

MirandaJ.M.D.PassosF.C. (2005). Composição e dinâmica de grupos Alouatta guariba clamitans Cabrera (Primates, Atelidae) em florest ombrófila mista no estado do Paraná, Brasil. — Rev. Bras. Zool. 22: 99-106.

MitaniJ.WattsD.PepperJ.MerriwetherD.A. (2002). Demographic and social constraints on male chimpanzee behaviour. — Anim. Behav. 63: 727-737.

MorinP.A.ChambersK.E.BoeschC.VigilantL. (2001). Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). — Mol. Ecol. 10: 1835-1844.

MunizL.VigilantL. (2008). Isolation and characterization of microsatellite markers in the white-faced capuchin monkey (Cebus capucinus) and cross-species amplification in other new World monkeys. — Mol. Ecol. Resour. 8: 402-405.

NevilleM.K. (1972). Social relationships within troops of red howler monkeys (Alouatta seniculus). — Folia Primatol. 18: 47-77.

OklanderL.I.KowalewskiM.M.CorachD. (2010). Genetic consequences of habitat fragmentation in black-and-gold howler (Alouatta caraya) population from Northern Argentina. — Int. J. Primatol. 31: 813-832.

OklanderL.I.KowalewskiM.CorachD. (2013). Male reproductive strategies in black and gold howler monkeys (Alouatta caraya). — Am. J. Primatol. 76: 43-55.

Perez-SweeneyB.M.Valladares-PaduaC.BurrellA.S.Di FioreA.SatkoskiJ.Van Coeverden-De GrootP.J.BoagP.T.MelnickD.J. (2005). Dinucleotide microsatellite primers designed for a critically endangered primate, the black lion tamarin (Leontopithecus chrysopygus). — Mol. Ecol. Notes 5: 198-201.

PerryS.MansonJ.H.MunizL.Gros-LouisJ.VigilantL. (2008). Kin-biased social behaviour in wild adult female white-faced capuchins, Cebus capucinus. — Anim. Behav. 76: 187-199.

PopeT.R. (1990). The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multi-male and single-male troops using genetic markers. — Behav. Ecol. Sociobiol. 27: 439-446.

PopeT.R. (1992). The influence of dispersal patterns and mating system on genetic differentiation within and between populations of the red howler monkey (Alouatta seniculus). — Evolution 46: 1112-1128.

PopeT.R. (1998). Effects of demography changes on group kinship structure and gene dynamics of populations of red howling monkeys. — J. Mammal. 79: 692-712.

PopeT.R. (2000a). Reproductive success increases with degree of kinship in cooperative coalitions of female red howler monkeys (Alouatta seniculus). — Behav. Ecol. Sociobiol. 48: 253-267.

PopeT.R. (2000b). The evolution of male philopatry in Neotropical monkeys. — In: Primate males: causes and consequences of variation in group composition ( KappelerP.M. ed.). Cambridge University PressCambridge p.  219-235.

PuseyA.E.PackerC. (1987). The evolution of sex-biased dispersal in lions. — Behaviour 101: 275-310.

QuellerD.C.GoodnightK.F. (1989). Estimating relatedness using genetic markers. — Evolution 43: 258-275.

RaymondM.RoussetF. (1995). GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism. — J. Hered. 86: 248-249.

RossiterS.J.JonesG.RansomeR.D.BarrattE.M. (2002). Relatedness structure and kin-biased foraging in the greater horseschoe bat (Rhinolophus ferrumequinum). — Behav. Ecol. Sociobiol. 51: 510-518.

RoussetF. (2008). Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. — Mol. Ecol. Resources 8: 103-106.

RumizD.I. (1990). Alouatta caraya: population density and demography in northern Argentina. — Am. J. Primatol. 21: 279-294.

SchoofV.A.M.JackK.M.IsbellL.A. (2009). What traits promote male parallel dispersal in primates?Behaviour 146: 701-726.

SilkJ.B. (2009). Nepotistic cooperation in non-human primate groups. — Phil. Trans. Roy. Soc. B 364: 3243-3254.

SteenbeekR.SterckE.H.M.de VriesH.van HooffJ.A.R.A.M. (2000). Costs and benefits of the one-male, age-graded, and all-male phases in wild Thomas’s langur groups. — In: Primate males: causes and consequences of variation in group composition ( KappelerP.M. ed.). Cambridge University PressCambridge p.  130-145.

StrierK.B.ChavesP.B.MendesS.L.FagundesV.Di FioreA. (2011). Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate. — Proc. Natl. Acad. Sci. USA 108: 18915-18919.

TaberletP.GriffinS.GoossensB.QuestiauS.ManceauV.EscaravageN.WaitsL.P.BouvetJ. (1996). Reliable genotyping of samples with very low DNA quantities using PCR. — Nucl. Acids Res. 24: 3189-3194.

Van BelleS.EstradaA. (2006). Demographic features of Alouatta pigra populations in extensive and fragmented forests. — In: New perspectives in the study of Mesoamerican primates: distribution ecology behavior and conservation ( EstradaA.GarberP.A.PavelkaM.S.M.LeuckeL.G. eds). Springer PressNew York, NY p.  121-142.

Van BelleS.EstradaA.StrierK.B. (2008). Social relationships among male Alouatta pigra. — Int. J. Primatol. 29: 1481-1498.

Van BelleS.KulpA.Thiessen-BockR.GraciaM.EstradaA. (2010). Observed infanticides following a male migration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. — Primates 51: 279-284.

Van BelleS.EstradaA.StrierK.B. (2011). Insights into social relationships among female black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. — Curr. Zool. 57: 1-7.

Van BelleS.EstradaA.StrierK.B.Di FioreA. (2012). Genetic structure and kinships patterns in a population of black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. — Am. J. Primatol. 74: 948-957.

WangE.MiltonK. (2003). Intragroup social relationships of male Alouatta palliata on Barro Colorado Island, Republic of Panama. — Int. J. Primatol. 24: 1227-1243.

WattsD.P. (1994). Social relationships of resident and immigrant female mountain gorillas, II. Female–female relationships. — Am. J. Primatol. 32: 13-30.

WattsD.P. (2001). Social relationships of female mountain gorillas. — In: Mountain gorillas: three decades of research at Karisoke ( RobbinsM.M.SicotteP.StewartK.J. eds). Cambridge University PressCambridge p.  215-240.

WeberJ.L.MayP.E. (1989). Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. — Am. J. Hum. Genet. 44: 388-396.

WeberJ.L.KwitekA.E.MayP.E. (1990). Dinucleotide repeat polymorphisms at the D5S107, D5S108, D5S111, D5S117 and D5S118 loci. — Nucleic Acids Res. 18: 4035.

WeissenbachJ.GyapayG.DibC.VignalA.MorissetteJ.MillaseauP.VaysseixG.LathtropM. (1992). A second-generation linkage map of the human genome. — Nature 359: 794-801.

ZuckerE.L.ClarkeM.R. (1998). Agonistic and affiliative relationships of adult female howlers (Alouatta palliata) in Costa Rica over a 4-year period. — Int. J. Primatol. 19: 433-449.

Figures

  • View in gallery

    Map of Palenque National Park showing the distribution of primary tropical rainforest (597 ha), secondary rain forest (300 ha) and human-induced pasture land (274 ha). Locations of the home ranges of the five study groups are indicated.

  • View in gallery

    Composition of the three study groups (Balam, Pakal and Motiepa) observed during a first observation period (September 2010–December 2011) and of the two study groups (Bolas and Unites) observed during a second observation period (March 2012–February 2013). Open circles represent disappearance of group members, black circles represent immigration of new group members. Dotted lines indicate periods excluded from the analyses. All study groups had infants and juveniles that were excluded from the analyses and are not presented in the figure. AM, adult male; SAM, sub-adult male; AF, adult female; SAF, sub-adult female; JM, juvenile male; JF, juvenile females.

  • View in gallery

    Social relationships and genetic relatedness among group members according to dyad type: (a) Mean ± SE percentage of time dyads spent within 1 m of each other, (b) Mean ± SE rates of affiliative interactions (s/h), (c) Mean ± SE rates of agonistic interactions (bouts/h), (d) Mean ± SE estimated r values. AM = adult male, SAM = sub-adult male, AF = adult female, SAF = sub-adult female.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 10 10 5
Full Text Views 6 6 6
PDF Downloads 0 0 0
EPUB Downloads 0 0 0