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Kinship, association, and social complexity in bats

  • Gerald S. WilkinsonEmail author
  • Gerald Carter
  • Kirsten M. Bohn
  • Barbara Caspers
  • Gloriana Chaverri
  • Damien Farine
  • Linus Günther
  • Gerald Kerth
  • Mirjam Knörnschild
  • Frieder Mayer
  • Martina Nagy
  • Jorge Ortega
  • Krista Patriquin
Original Article
Part of the following topical collections:
  1. Social complexity: patterns, processes, and evolution

Abstract

Among mammals, bats exhibit extreme variation in sociality, with some species living largely solitary lives while others form colonies of more than a million individuals. Some tropical species form groups during the day that persist throughout the year while many temperate species only gather into groups during hibernation or parturition. How groups form and then persist has now been described for a number of species, but the degree to which kinship explains patterns of association has never been quantified across species. Here, we use social network analysis and genetic data to determine the extent to which relatedness contributes to associations among individuals estimated from free-ranging animals across nine species from four families of bats. Network analysis reveals that all species show evidence of emergent social structure. Variation in the strength of the relationship between genetic relatedness and social association appears to be related to the degree of roost switching, i.e., species in which individuals change roosts frequently tend to exhibit higher levels of association among relatives. Sex-biased dispersal determines whether associations were between male or female relatives. The strength of associations among kin does not predict known occurrence of complex behaviors, such as dominance or various types of cooperation, indicating that kinship is not a prerequisite for social complexity in bats.

Significance statement

The number of differentiated relationships has been proposed as a way to measure social complexity. Among primates, relationships can be differentiated on the basis of rank, age, kinship, or association. Application of this approach to other groups of mammals that vary in sociality could help reveal ecological, behavioral, or cognitive similarities and differences between species. As a first step toward this approach, we used social network analysis on long-term individual records and estimated relatedness using genetic markers for nine species of bats. We confirmed nonrandom emergent social structure in all species. Kinship was predictive of social association among individuals of the same sex in a few species, but largely independent of the occurrence of complex behaviors, such as dominance among males or cooperation among females. Complex social behavior in bats appears to require frequent interactions among a small number of individuals that roost together for multiple years.

Keywords

Social networks Kinship Modularity Fission-fusion Cooperation 

Notes

Acknowledgments

We thank B. Negash for assistance in preparing data and H. Whitehead, D. Lukas, P. Kappeler, and two anonymous reviewers, as well as several other participants of the Göttinger Freilandtage, for useful suggestions.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

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References

  1. Aplin LM, Farine DR, Morand-Ferron J, Sheldon BC (2012) Social networks predict patch discovery in a wild population of songbirds. Proc R Soc Lond B 279:4199–4205CrossRefGoogle Scholar
  2. Archie EA, Moss CJ, Alberts SC (2006) The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc R Soc Lond B 273:513–522CrossRefGoogle Scholar
  3. Arnold BD (2011) Social vocalizations and their implications for group dynamics of pallid bats (Antrozous pallidus). Doctoral dissertation, University of MarylandGoogle Scholar
  4. Arnold BD, Wilkinson GS (2011) Individual specific contact calls of pallid bats (Antrozous pallidus) attract conspecifics at roosting sites. Behav Ecol Sociobiol 65:1581–1593CrossRefGoogle Scholar
  5. Arnold BD, Wilkinson GS (2015) Female natal philopatry and gene flow between divergent clades of pallid bats (Antrozous pallidus). J Mammal 96:531–540CrossRefGoogle Scholar
  6. August TA, Nunn MA, Fensome AG, Linton DM, Mathews F (2014) Sympatric woodland Myotis bats form tight-knit social groups with exclusive roost home ranges. PLoS One 9:e112225PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aureli F, Schaffner CM, Boesch C et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654Google Scholar
  8. Avilés L, Harwood G (2012) A quantitative index of sociality and its application to group living spiders and other social organisms. Ethology 118:1219–1229PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bell MBV, Nichols HJ, Gilchrist JS, Cant MA, Hodge SJ (2012) The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses. Proc R Soc Lond B 279:619–624CrossRefGoogle Scholar
  10. Bell MBV, Cant MA, Borgeaud C, Thavarajah N, Samson J, Clutton-Brock TH (2014) Suppressing subordinate reproduction provides benefits to dominants in cooperative societies of meerkats. Nat Commun 5:4499PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bennett NC, Faulkes CG, Molteno AJ (1996) Reproductive suppression in subordinate, non-breeding female Damaraland mole-rats: two components to a lifetime of socially induced infertility. Proc R Soc Lond B 263:1599–1603CrossRefGoogle Scholar
  12. Bergman TJ, Beehner JC (2015) Measuring social complexity. Anim Behav 103:203–209CrossRefGoogle Scholar
  13. Blackwood JC, Streicker DG, Altizer S, Rohani P (2013) Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats. Proc Natl Acad Sci U S A 110:20837–20842PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bohn KM, Moss CF, Wilkinson GS (2009) Pup guarding by greater spear-nosed bats. Behav Ecol Sociobiol 63:1693–1703CrossRefGoogle Scholar
  15. Bouchard S (2001) Sex discrimination and roostmate recognition by olfactory cues in the African bats, Mops condylurus and Chaerephon pumilus (Chiroptera: Molossidae). J Zool 254:109–117CrossRefGoogle Scholar
  16. Boughman JW (1997) Greater spear-nosed bats give group-distinctive calls. Behav Ecol Sociobiol 40:61–70CrossRefGoogle Scholar
  17. Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalizations. Anim Behav 55:1717–1732PubMedCrossRefPubMedCentralGoogle Scholar
  18. Bradbury JW (1977) Social organization and communication. In: Wimsatt WA (ed) The biology of bats. Academic Press, New York, pp 1–72Google Scholar
  19. Bradbury JW, Vehrencamp SL (1976) Social organization and foraging in emballonurid bats. I. Field studies. Behav Ecol Sociobiol 1:337–381CrossRefGoogle Scholar
  20. Brent LJ, Franks DW, Foster EA, Balcomb KC, Cant MA, Croft DP (2015) Ecological knowledge, leadership, and the evolution of menopause in killer whales. Curr Biol 25:746–750PubMedCrossRefPubMedCentralGoogle Scholar
  21. Brooke AP, Decker DM (1996) Lipid compounds in secretions of fishing bat, Noctilio leporinus (Chiroptera: Noctilionidae). J Chem Ecol 22:1411–1428PubMedCrossRefPubMedCentralGoogle Scholar
  22. Buchalski MR, Chaverri G, Vonhof MJ (2014) When genes move farther than offspring: gene flow by male gamete dispersal in the highly philopatric bat species Thyroptera tricolor. Mol Ecol 23:464–480PubMedCrossRefPubMedCentralGoogle Scholar
  23. Carter G, Leffer L (2015) Social grooming in bats: are vampire bats exceptional? PLoS One 10:e0138430PubMedPubMedCentralCrossRefGoogle Scholar
  24. Carter GG, Wilkinson GS (2013a) Cooperation and conflict in the social lives of bats. In: Adams RA, Pedersen SC (eds) Bat evolution, ecology, and conservation. Springer Science Press, New York, pp 225–242CrossRefGoogle Scholar
  25. Carter GG, Wilkinson GS (2013b) Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proc R Soc Lond B 280:20122573CrossRefGoogle Scholar
  26. Carter GG, Wilkinson GS (2016) Common vampire bat contact calls attract past food-sharing partners. Anim Behav 116:45–51CrossRefGoogle Scholar
  27. Carter GG, Logsdon R, Arnold BD, Menchaca A, Medellin RA (2012) Adult vampire bats produce contact calls when isolated: acoustic variation by species, population, colony, and individual. PLoS One 7:e38791PubMedPubMedCentralCrossRefGoogle Scholar
  28. Carter KD, Brand R, Carter JK, Shorrocks B, Goldizen AW (2013) Social networks, long-term associations and age-related sociability of wild giraffes. Anim Behav 86:901–910CrossRefGoogle Scholar
  29. Castella V, Ruedi M, Excoffier L (2001) Contrasted patterns of mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis. J Evol Biol 14:708–720CrossRefGoogle Scholar
  30. Chapais B (1995) Alliances as a means of competition in primates: evolutionary, developmental, and cognitive aspects. Yearb Phys Anthropol 38:115–136CrossRefGoogle Scholar
  31. Chaverri G (2010) Comparative social network analysis in a leaf-roosting bat. Behav Ecol Sociobiol 64:1619–1630CrossRefGoogle Scholar
  32. Chaverri G, Gillam EH (2015) Repeatability in the contact calling system of Spix’s disc-winged bat (Thyroptera tricolor). R Soc Open Sci 2:140197PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chaverri G, Kunz TH (2011) All-offspring natal philopatry in a neotropical bat. Anim Behav 82:1127–1133CrossRefGoogle Scholar
  34. Chaverri G, Gillam EH, Vonhof MJ (2010) Social calls used by a leaf-roosting bat to signal location. Biol Lett 6:441–444PubMedPubMedCentralCrossRefGoogle Scholar
  35. Chaverri G, Gillam EH, Kunz TH (2013) A call-and-response system facilitates group cohesion among disc-winged bats. Behav Ecol 24:481–487CrossRefGoogle Scholar
  36. Chen S-F, Jones G, Rossiter SJ (2008) Sex-biased gene flow and colonization in the Formosan lesser horseshoe bat: inference from nuclear and mitochondrial markers. J Zool 274:207–215CrossRefGoogle Scholar
  37. Clutton-Brock TH, Lukas D (2012) The evolution of social philopatry and dispersal in female mammals. Mol Ecol 21:472–492PubMedCrossRefGoogle Scholar
  38. Clutton-Brock TH, Russell AF, Sharpe LL, Brotherton PNM, McIlrath GM, White S, Cameron EZ (2001) Effects of helpers on juvenile development and survival in meerkats. Science 293:2446–2449PubMedCrossRefGoogle Scholar
  39. Clutton-Brock TH, Hodge SJ, Flower TP, Spong GF, Young AJ (2010) Adaptive suppression of subordinate reproduction in cooperative mammals. Am Nat 176:664–673PubMedCrossRefGoogle Scholar
  40. Connor RC, Smolker RA, Richards AF (1992) Two levels of alliance formation among male bottle-nosed dolphins (Tursiops sp.). Proc Natl Acad Sci U S A 89:987–990PubMedPubMedCentralCrossRefGoogle Scholar
  41. Connor RC, Mann J, Tyack PL, Whitehead H (1998) Social evolution in toothed whales. Trends Ecol Evol 13:228–232PubMedCrossRefGoogle Scholar
  42. Craft ME (2015) Infectious disease transmission and contact networks in wildlife and livestock. Phil Trans R Soc B 370:20140107PubMedCrossRefGoogle Scholar
  43. Creel SR, Creel NM (1991) Energetics, reproductive suppression and obligate communal breeding in carnivores. Behav Ecol Sociobiol 28:263–270CrossRefGoogle Scholar
  44. Creel S, Creel NM, Mills MGL, Monfort SL (1997) Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav Ecol 8:298–306CrossRefGoogle Scholar
  45. Dechmann DKN, Kalko EKV, Kerth G (2007) All-offspring dispersal in a tropical mammal with resource defense polygyny. Behav Ecol Sociobiol 61:1219–1228CrossRefGoogle Scholar
  46. Defanis E, Jones G (1995) The role of odor in the discrimination of conspecifics by pipistrelle bats. Anim Behav 49:835–839CrossRefGoogle Scholar
  47. Dunbar RIM (1983) Structure of gelada baboon reproductive units. 2. Social relationships between reproductive females. Anim Behav 31:556–564CrossRefGoogle Scholar
  48. Englert AC, Greene MJ (2009) Chemically-mediated roostmate recognition and roost selection by Brazilian free-tailed bats (Tadarida brasiliensis). PLoS One 4:e7781PubMedPubMedCentralCrossRefGoogle Scholar
  49. Farine DR (2013) Animal social network inference and permutations for ecologists in R using asnipe. Methods Ecol Evol 4:1187–1194CrossRefGoogle Scholar
  50. Farine DR (2017) A guide to null models for animal social network analysis. Methods Ecol Evol 8:1309–1320PubMedPubMedCentralCrossRefGoogle Scholar
  51. Farine DR, Sheldon BC (2016) Social ecology of a woodland songbird community: from individual movements to the emergence of population social structure. bioRxiv.  https://doi.org/10.1101/085944
  52. Farine DR, Whitehead H (2015) Constructing, conducting and interpreting animal social network analysis. J Anim Ecol 84:1144–1163PubMedPubMedCentralCrossRefGoogle Scholar
  53. Fortuna MA, Popa-Lisseanu AG, Ibáñez C, Bascompte J (2009) The roosting spatial network of a bird-predator bat. Ecology 90:934–944PubMedCrossRefGoogle Scholar
  54. Freeberg TM, Dunbar RI, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philos Trans R Soc B 367:1785–1801CrossRefGoogle Scholar
  55. Gager Y, Gimenez O, O'Mara MT, Dechmann DKN (2016) Group size, survival and surprisingly short lifespan in socially foraging bats. BMC Ecol 16:2PubMedPubMedCentralCrossRefGoogle Scholar
  56. Garg KM, Chattopadhyay B, Ramakrishnan U (2018) Social structure in the harem-forming promiscuous fruit bat, Cynopterus sphinx, is the harem truly important? R Soc Open Sci 5:172024PubMedPubMedCentralCrossRefGoogle Scholar
  57. Gillam EH, Chaverri G (2012) Strong individual signatures and weaker group signatures in contact calls of Spix’s disc-winged bat, Thyroptera tricolor. Anim Behav 83:269–276CrossRefGoogle Scholar
  58. Gillam EH, Chaverri G, Montero K, Sagot M (2013) Social calls produced within and near the roost in two species of tent-making bats, Dermanura watsoni and Ectophylla alba. PLoS One 8:e61731PubMedPubMedCentralCrossRefGoogle Scholar
  59. Girvan M, Newman MEJ (2002) Community structure in social and biological networks. Proc Natl Acad Sci U S A 99:7821–7826PubMedPubMedCentralCrossRefGoogle Scholar
  60. Godinho LN, Lumsden LF, Coulson G, Griffiths SR (2015) Network analysis reveals cryptic seasonal patterns of association in Gould’s wattled bats (Chalinolobus gouldii) roosting in bat-boxes. Behaviour 152:1079–2105CrossRefGoogle Scholar
  61. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  62. Günther L, Lopez MD, Knörnschild M, Reid K, Nagy M, Mayer F (2016) From resource to female defence: the impact of roosting ecology on a bat’s mating strategy. R Soc Open Sci 3:160503PubMedPubMedCentralCrossRefGoogle Scholar
  63. He P, Maldonado-Chaparro A, Farine DR (2019) The role of habitat configuration in shaping social structure: a gap in studies of animal social complexity. Behav Ecol Sociobiol.  https://doi.org/10.1007/s00265-018-2602-7
  64. Heckel G, von Helversen O (2002) Male tactics and reproductive success in the harem polygynous bat Saccopteryx bilineata. Behav Ecol 13:750–756CrossRefGoogle Scholar
  65. Hoppitt W, Farine DR (2018) Association indices for quantifying social relationships: how to deal with missing observations of individuals or groups. Anim Behav 136:227–238CrossRefGoogle Scholar
  66. Jarvis JUM (1981) Eusociality in a mammal—cooperative breeding in naked mole-rat colonies. Science 212:571–573PubMedCrossRefGoogle Scholar
  67. Johnson N, Arechiga-Ceballos N, Aguilar-Setien A (2014) Vampire bat rabies: ecology, epidemiology and control. Viruses 6:1911–1928PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kappeler PM (2019) A framework for studying social complexity. Behav Ecol Sociobiol.  https://doi.org/10.1007/s00265-018-2601-8
  69. Kerth G (2008) Causes and consequences of sociality in bats. Bioscience 58:737–746CrossRefGoogle Scholar
  70. Kerth G, König B (1999) Fission, fusion and nonrandom associations in female Bechstein’s bats (Myotis bechsteinii). Behaviour 136:1187–1202CrossRefGoogle Scholar
  71. Kerth G, Morf L (2004) Behavioural and genetic data suggest that Bechstein’s bats predominantly mate outside the breeding habitat. Ethology 110:987–999CrossRefGoogle Scholar
  72. Kerth G, Reckardt K (2003) Information transfer about roosts in female Bechstein’s bats: an experimental field study. Proc R Soc Lond B 270:511–515CrossRefGoogle Scholar
  73. Kerth G, Safi K, König B (2002) Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein’s bat (Myotis bechsteinii). Behav Ecol Sociobiol 52:203–210CrossRefGoogle Scholar
  74. Kerth G, Perony N, Schweitzer F (2011) Bats are able to maintain long-term social relationships despite the high fission-fusion dynamics of their groups. Proc R Soc Lond B 278:2761–2767CrossRefGoogle Scholar
  75. Knörnschild M, Nagy M, Metz M, Mayer F, von Helversen O (2012) Learned vocal group signatures in the polygynous bat Saccopteryx bilineata. Anim Behav 84:761–769CrossRefGoogle Scholar
  76. Kudo H, Dunbar RIM (2001) Neocortex size and social network size in primates. Anim Behav 62:711–722CrossRefGoogle Scholar
  77. Lee PC (1987) Allomothering among African elephants. Anim Behav 35:278–291CrossRefGoogle Scholar
  78. Lewis SE (1995) Roost fidelity of bats: a review. J Mamm 76:481–496CrossRefGoogle Scholar
  79. Lewis SE (1996) Low roost-site fidelity in pallid bats: associated factors and effect on group stability. Behav Ecol Sociobiol 39:335–344CrossRefGoogle Scholar
  80. Lukas D, Clutton-Brock T (2012) Life histories and the evolution of cooperative breeding in mammals. Proc R Soc Lond B 279:4065–4070CrossRefGoogle Scholar
  81. MacKinnon KC, Fuentes A (2011) Primates, niche construction, and social complexity: the roles of social cooperation and altruism. In: Sussman RW, Cloninger CR (eds) Origins of altruism and cooperation. Springer, New York, pp 121–143CrossRefGoogle Scholar
  82. MacLeod KJ, Lukas D (2014) Revisiting non-offspring nursing: allonursing evolves when the costs are low. Biol Lett 10:20140378PubMedCentralCrossRefGoogle Scholar
  83. McComb K, Moss C, Durant SM, Baker L, Sayialel S (2001) Matriarchs as repositories of social knowledge in African elephants. Science 292:491–494PubMedCrossRefPubMedCentralGoogle Scholar
  84. McCracken GF (1987) Genetic structure of bat social groups. In: Racey PA, Fenton MB, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 281–298Google Scholar
  85. McCracken GF, Bradbury JW (1981) Social organization and kinship in the polygynous bat Phyllostomus hastatus. Behav Ecol Sociobiol 8:11–34CrossRefGoogle Scholar
  86. McCracken GF, Wilkinson GS (2000) Bat mating systems. In: Krutszch PH, Crichton EG (eds) Reproductive biology of bats. Academic Press, New York, pp 321–362CrossRefGoogle Scholar
  87. Metheny JD, Kalcounis-Rueppell MC, Willis CKR, Kolar KA, Brigham RM (2007) Genetic relationships between roost-mates in a fission–fusion society of tree-roosting big brown bats (Eptesicus fuscus). Behav Ecol Sociobiol 62:1043–1051CrossRefGoogle Scholar
  88. Moehlman PD, Hofer H (1997) Cooperative breeding, reproductive suppression, and body mass in canids. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, New York, pp 76–128Google Scholar
  89. Moller LM, Beheregaray LB, Harcourt RG, Krutzen M (2001) Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Proc R Soc Lond B 268:1941–1947CrossRefGoogle Scholar
  90. Morrison DW (1979) Apparent male defense of tree hollows in the bat, Artibeus jamaicensis. J Mammal 60:11–15CrossRefGoogle Scholar
  91. Moussy C, Hosken DJ, Mathews F, Smith GC, Aegerter JN, Bearhop S (2013) Migration and dispersal patterns of bats and their influence on genetic structure. Mamm Rev 43:183–195CrossRefGoogle Scholar
  92. Nagy M, Knörnschild M, Voigt CC, Mayer F (2012) Male greater sac-winged bats gain direct fitness benefits when roosting in multimale colonies. Behav Ecol 23:597–606CrossRefGoogle Scholar
  93. Nagy M, Günther L, Knörnschild M, Mayer F (2013) Female-biased dispersal in a bat with a female-defence mating strategy. Mol Ecol 22:1733–1745PubMedCrossRefPubMedCentralGoogle Scholar
  94. Newman MEJ (2004) Analysis of weighted networks. Phys Rev E 70:056131CrossRefGoogle Scholar
  95. Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci U S A 103:8577–8582PubMedPubMedCentralCrossRefGoogle Scholar
  96. Omer DB, Maimon SR, Las L, Ulanovsky N (2018) Social place-cells in the bat hippocampus. Science 359:218–224PubMedCrossRefPubMedCentralGoogle Scholar
  97. Ortega J, Arita HT (2000) Defence of females by dominant males of Artibeus jamaicensis (Chiroptera: Phyllostomidae). Ethology 106:395–407CrossRefGoogle Scholar
  98. Ortega J, Maldonado JE, Wilkinson GS, Arita HT, Fleischer RC (2003) Male dominance, paternity, and relatedness in the Jamaican fruit-eating bat (Artibeus jamaicensis). Mol Ecol 12:2409–2415PubMedCrossRefPubMedCentralGoogle Scholar
  99. Packer C, Lewis S, Pusey A (1992) A comparative analysis of nonoffspring nursing. Anim Behav 43:265–281CrossRefGoogle Scholar
  100. Park SR (1991) Development of social structure in a captive colony of the common vampire bat, Desmodus rotundus. Ethology 89:335–341CrossRefGoogle Scholar
  101. Parsons KM, Durban JW, Claridge DE, Balcomb KC, Noble LR, Thompson PM (2003) Kinship as a basis for alliance formation between male bottlenose dolphins, Tursiops truncatus, in the Bahamas. Anim Behav 66:185–194CrossRefGoogle Scholar
  102. Parsons KM, Balcomb KC, Ford JKB, Durban JW (2009) The social dynamics of southern resident killer whales and conservation implications for this endangered population. Anim Behav 77:963–971CrossRefGoogle Scholar
  103. Parsons JG, SKA R, Shilton LA (2011) Roost fidelity in spectacled flying-foxes Pteropus conspicillatus: implications for conservation and management. In: Law B, Eby P, Lunney D, Lumsden L (eds) The biology and conservation of Australasian bats. Royal Zoological Society of NSW, Mosman, pp 66–71CrossRefGoogle Scholar
  104. Pasquaretta C, Leve M, Claidiere N et al (2014) Social networks in primates: smart and tolerant species have more efficient networks. Sci Rep 4:7600PubMedPubMedCentralCrossRefGoogle Scholar
  105. Patriquin KJ, Leonard ML, Broders HG, Garroway CJ (2010) Do social networks of female northern long-eared bats vary with reproductive period and age? Behav Ecol Sociobiol 64:899–913CrossRefGoogle Scholar
  106. Patriquin KJ, Palstra F, Leonard ML, Broders HG (2013) Female northern myotis (Myotis septentrionalis) that roost together are related. Behav Ecol 24:949–954CrossRefGoogle Scholar
  107. Payne K (2003) Sources of social complexity in the three elephant species. In: de Waal FBM, Tyack PL (eds) Animal social complexity. Harvard University Press, Cambridge, pp 57–85Google Scholar
  108. Podgorski T, Lusseau D, Scandura M, Sonnichsen L, Jedrzejewska B (2014) Long-lasting, kin-directed female interactions in a spatially structured wild boar social network. PLoS One 9:e99875PubMedPubMedCentralCrossRefGoogle Scholar
  109. Pretzlaff I, Kerth G, Dausmann KH (2010) Communally breeding bats use physiological and behavioural adjustments to optimise daily energy expenditure. Naturwissenschaften 97:353–363PubMedPubMedCentralCrossRefGoogle Scholar
  110. Racey PA, Entwhistle AC (2000) Life history and reproductive strategies of bats. In: Krutzsch PH, Crichton EG (eds) Reproductive biology of bats. Academic Press, New York, pp 363–414CrossRefGoogle Scholar
  111. Roberts BJ, Catterall CP, Eby P, Kanowski J (2012) Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management. PLoS One 7:e42532PubMedPubMedCentralCrossRefGoogle Scholar
  112. Rossiter SJ, Jones G, Ransome RD, Barratt EM (2002) Relatedness structure and kin-biased foraging in the greater horseshoe bat (Rhinolophus ferrumequinum). Behav Ecol Sociobiol 51:510–518CrossRefGoogle Scholar
  113. Roulin A (2002) Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence. Anim Behav 63:201–208CrossRefGoogle Scholar
  114. Safi K, Kerth G (2003) Secretions of the interaural gland contain information about individuality and colony membership in the Bechstein’s bat. Anim Behav 65:363–369CrossRefGoogle Scholar
  115. Sah P, Leu ST, Cross PC, Hudson PJ, Bansal S (2017) Unraveling the disease consequences and mechanisms of modular structure in animal social networks. Proc Natl Acad Sci U S A 114:4165–4170PubMedPubMedCentralCrossRefGoogle Scholar
  116. Schino G, Aureli F (2010) The relative roles of kinship and reciprocity in explaining primate altruism. Ecol Lett 13:45–50PubMedCrossRefGoogle Scholar
  117. Schöner CR, Schöner MG, Kerth G (2010) Similar is not the same: social calls of conspecifics are more effective in attracting wild bats to day roosts than those of other bat species. Behav Ecol Sociobiol 64:2053–2063CrossRefGoogle Scholar
  118. Seyfarth RM, Cheney DL (1984) Grooming, alliances and reciprocal altruism in vervet monkeys. Nature 308:541–543PubMedCrossRefPubMedCentralGoogle Scholar
  119. Shizuka D, Farine DR (2016) Measuring the robustness of network community structure using assortativity. Anim Behav 112:237–246PubMedPubMedCentralCrossRefGoogle Scholar
  120. Silk JB (2007) Social components of fitness in primate groups. Science 317:1347–1351PubMedCrossRefPubMedCentralGoogle Scholar
  121. Silk JB, Alberts SC, Altmann J (2004) Patterns of coalition formation by adult female baboons in Amboseli, Kenya. Anim Behav 67:573–582CrossRefGoogle Scholar
  122. Storz JF (2000) Social structure of a polygynous tent-making bat, Cynopterus sphinx (Megachiroptera). J Zool 251:151–165CrossRefGoogle Scholar
  123. Storz JF, Bhat HR, Kunz TH (2001a) Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. I. Inbreeding, outbreeding, and population subdivision. Evolution 55:1215–1223PubMedCrossRefPubMedCentralGoogle Scholar
  124. Storz JF, Bhat HR, Kunz TH (2001b) Genetic consequences of polygyny and social structure in an Indian fruit bat, Cynopterus sphinx. II. Variance in male mating success and effective population size. Evolution 55:1224–1232PubMedCrossRefGoogle Scholar
  125. Trune DR, Slobodchikoff CN (1976) Social effects of roosting on the metabolism of the pallid bat (Antrozous pallidus). J Mammal 57:656–663PubMedCrossRefPubMedCentralGoogle Scholar
  126. Tuttle MD, Stevenson D (1982) Growth and survival of bats. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 105–150CrossRefGoogle Scholar
  127. Wang J (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145PubMedCrossRefGoogle Scholar
  128. Wang J (2017) Estimating pairwise relatedness in a small sample of individuals. Heredity 119:302–313PubMedPubMedCentralCrossRefGoogle Scholar
  129. Whitehead H (1995) Investigating structure and temporal scale in social organizations using identified individuals. Behav Ecol 6:199–208CrossRefGoogle Scholar
  130. Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. Chicago University Press, ChicagoCrossRefGoogle Scholar
  131. Whitehead H (2009) SOCPROG programs: analysing animal social structures. Behav Ecol Sociobiol 63:765–778CrossRefGoogle Scholar
  132. Wilkinson GS (1984) Reciprocal food sharing in vampire bats. Nature 309:181–184CrossRefGoogle Scholar
  133. Wilkinson GS (1985a) The social organization of the common vampire bat. I. Pattern and cause of association. Behav Ecol Sociobiol 17:111–121Google Scholar
  134. Wilkinson GS (1985b) The social organization of the common vampire bat. II. Mating system, genetic structure, and relatedness. Behav Ecol Sociobiol 17:123–134Google Scholar
  135. Wilkinson GS (1986) Social grooming in the common vampire bat, Desmodus rotundus. Anim Behav 34:1880–1889CrossRefGoogle Scholar
  136. Wilkinson GS (1987) Altruism and cooperation in bats. In: Racey PA, Fenton MB, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 299–323Google Scholar
  137. Wilkinson GS (1992a) Communal nursing in evening bats. Behav Ecol Sociobiol 31:225–235CrossRefGoogle Scholar
  138. Wilkinson GS (1992b) Information transfer at evening bat colonies. Anim Behav 44:501–518CrossRefGoogle Scholar
  139. Wilkinson GS, Boughman JW (1998) Social calls coordinate foraging in greater spear-nosed bats. Anim Behav 55:337–350PubMedCrossRefGoogle Scholar
  140. Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1:124–131PubMedCrossRefGoogle Scholar
  141. Wilkinson GS, Carter GG, Bohn KM, Adams DM (2016) Non-kin cooperation in bats. Philos Trans R Soc B 371:20150095CrossRefGoogle Scholar
  142. Wiszniewski J, Brown C, Moller LM (2012) Complex patterns of male alliance formation in a dolphin social network. J Mammal 93:239–250CrossRefGoogle Scholar
  143. Wittemyer G, Okello JB, Rasmussen HB, Arctander P, Nyakaana S, Douglas-Hamilton I, Siegismund HR (2009) Where sociality and relatedness diverge: the genetic basis for hierarchical social organization in African elephants. Proc R Soc Lond B 276:3513–3521CrossRefGoogle Scholar
  144. Worthington-Wilmer J, Barratt EM (1996) A non-lethal method of tissue sampling for genetic studies of chiropterans. Bat Res News 37:1–3Google Scholar
  145. Zeus VM, Reusch C, Kerth G (2018) Long-term roosting data reveal a unimodular social network in large fission-fusion society of the colony-living Natterer’s bat (Myotis nattereri). Behav Ecol Sociobiol 72:99–112CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Gerald S. Wilkinson
    • 1
    Email author
  • Gerald Carter
    • 2
    • 3
    • 4
  • Kirsten M. Bohn
    • 5
  • Barbara Caspers
    • 6
  • Gloriana Chaverri
    • 7
  • Damien Farine
    • 2
    • 3
  • Linus Günther
    • 8
  • Gerald Kerth
    • 9
  • Mirjam Knörnschild
    • 8
    • 10
    • 11
  • Frieder Mayer
    • 8
  • Martina Nagy
    • 10
  • Jorge Ortega
    • 12
  • Krista Patriquin
    • 13
  1. 1.Department of BiologyUniversity of MarylandCollege ParkUSA
  2. 2.Department of Collective BehaviourMax Planck Institut für OrnithologieKonstanzGermany
  3. 3.Department of BiologyUniversity of KonstanzKonstanzGermany
  4. 4.Department of Evolution, Ecology, and Organismal BiologyThe Ohio State UniversityColumbusUSA
  5. 5.Department of Psychological and Brain SciencesJohns Hopkins UniversityBaltimoreUSA
  6. 6.Department of Animal BehaviourBielefeld UniversityBielefeldGermany
  7. 7.Recinto de GolfitoUniversidad de Costa RicaGolfitoCosta Rica
  8. 8.Museum für NaturkundeBerlinGermany
  9. 9.Zoologisches Institut und MuseumGreifswaldGermany
  10. 10.Freie Universitat BerlinBerlinGermany
  11. 11.Smithsonian Tropical Research InstituteBalboaPanama
  12. 12.Laboratorio de Bioconservación y Manejo, Posgrado en Ciencias Quimicobiológicas, Departamento de Zoología, Escuela Nacional de Ciencias BiológicasInstituto Politécnico NacionalMexico CityMexico
  13. 13.University of Toronto MississaugaMississaugaCanada

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