Skip to main content
Log in

Selection on social traits in greater spear-nosed bats, Phyllostomus hastatus

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Many studies assume that selection molds social traits and have investigated the manner in which this occurs, yet very few studies have measured the strength of selection on social traits in natural populations. In this paper, I report results of phenotypic selection analyses on two social traits – the size of social groups and the frequency of group foraging – in Phyllostomus hastatus, the greater spear-nosed bat. I found significant positive directional selection on individual group foraging frequency, but no directional selection on individuals in different-sized social groups. These results have implications for the structure of social groups, cooperative behavior among group mates, and maternal investment strategies. I argue that combining studies of natural selection on wild populations with experiments to identify the agents and mechanisms of selection can do much to increase our understanding of social evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arlettaz R, Christe P, Lugon A, Perrin N, Vogel P (2001) Food availability dictates the timing of parturition in insectivorous mouse-eared bats. Oikos 95:105–111

    Google Scholar 

  • Armitage KB (1986) Marmot polygyny revisited: determinants of male and female reproductive strategies. In: Rubenstein DI, Wrangham RW (eds) Ecological aspects of social evolution. Princeton University Press, Princeton, NJ, pp 303–331

    Google Scholar 

  • Arnold SJ, Wade MJ (1984) On the measurement of natural and sexual selection: theory. Evolution 38:709–719

    Google Scholar 

  • Barnard CJ, Sibly RM (1981) Producers and scroungers: a general model and its application to captive flocks of house sparrows. Anim Behav 29:543–550

    Google Scholar 

  • Beauchamp G, Fernandez-Juricic E (2005) The group-size paradox: effects of learning and patch departure rules. Behav Ecol 16:352–357

    Google Scholar 

  • Boughman JW (1997) Greater spear-nosed bats give group-distinctive calls. Behav Ecol Sociobiol 40:61–70

    Google Scholar 

  • Boughman JW (1998) Vocal learning by greater spear-nosed bats. Proc R Soc Lond B 265:227–233

    CAS  Google Scholar 

  • Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalizations. Anim Behav 55:1717–1732

    PubMed  Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Bradbury JW, Vehrencamp SL (1976) Social organization and foraging in emballonurid bats. II. A model for the determination of group size. Behav Ecol and Sociobiol 1:383–404

    Google Scholar 

  • Brown CR (1988) Enhanced foraging efficiency through information centers: a benefit of coloniality in cliff swallows. Ecology 69:602–613

    Google Scholar 

  • Brown CR, Brown MB (1996) Coloniality in the cliff swallow: the effect of group size on social behavior. Chicago University Press, Chicago, IL

    Google Scholar 

  • Brown CR, Brown MB (2004) Group size and ectoparasitism affect daily survival probability in a colonial bird. Behav Ecol Sociobiol 56:498–511

    Google Scholar 

  • Burland TM, Wilmer JW (2001) Seeing in the dark: molecular approaches to the study of bat populations. Biol Rev 76:389–409

    PubMed  CAS  Google Scholar 

  • Burland TM, Barratt EM, Nichols RA, Racey PA (2001) Mating patterns, relatedness and the basis of natal philopatry in the brown long-eared bat, Plecotus auritus. Mol Ecol 10:1309–1321

    PubMed  CAS  Google Scholar 

  • Caraco T (1980) Stochastic dynamics of avian foraging flocks. Am Nat 115:262–275

    Google Scholar 

  • Caraco T (1981) Risk-sensitivity and foraging groups. Ecology 62:527–531

    Google Scholar 

  • Caraco T, Giraldeau L-A (1991) Social foraging: producing and scrounging in a stochastic environment. J Theor Biol 153:559–583

    Google Scholar 

  • Caraco T, Barkan C, Beacham JL, Brisbin L, Lima SL, Mohan A, Newman JA, Webb W, Withiam ML (1989) Dominance and social foraging: a laboratory study. Anim Behav 38:41–58

    Google Scholar 

  • Carriere Y, Roitberg BD (1996) Optimality modelling and quantitative genetics as alternatives to study the evolution of foraging behaviours in insect herbivores. Evol Ecol 10:289–305

    Google Scholar 

  • Cheney DL (1981) Intergroup encounters among free-ranging vervet monkeys. Folia Primatol 35:124–146

    PubMed  CAS  Google Scholar 

  • Clark CW, Mangel M (1984) Foraging and flocking strategies: information in an uncertain environment. Am Nat 123:626–641

    Google Scholar 

  • Clark CW, Mangel M (1986) The evolutionary advantages of group foraging. Theor Popul Biol 30:45–75

    Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success. University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Clutton-Brock TH (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72

    PubMed  CAS  Google Scholar 

  • Clutton-Brock TH, Godfray C (1991) Parental investment. In: Krebs JR, Davies NB (eds) Behavioural ecology, 3rd edn. Blackwell, Oxford, pp 234–262

    Google Scholar 

  • 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 293:2446–2449

    PubMed  CAS  Google Scholar 

  • Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Ann Rev Ecolog Syst 29:141–177

    Google Scholar 

  • Connor RC (1995a) Altruism among non-relatives: alternatives to the ‘prisoner’s dilemma’. Trends Ecol Evol 10:84–86

    Google Scholar 

  • Connor RC (1995b) The benefits of mutualism—a conceptual-framework. Biol Rev Camb Philos Soc 70:427–457

    Google Scholar 

  • Cote SD, Festa-Bianchet M (2001) Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 127:230–238

    Google Scholar 

  • Creel SR, Macdonald DW (1995) Sociality, group size and reproductive suppression among carnivores. Adv Study Behav 24:203–257

    Article  Google Scholar 

  • Cumming GS, Bernard RTF (1997) Rainfall, food abundance and timing of parturition in African bats. Oecologia 111:309–317

    Google Scholar 

  • Dubois F, Giraldeau L-A (2003) The forager’s dilemma: food sharing and food defense as risk-sensitive foraging options. Am Nat 162:768–779

    PubMed  Google Scholar 

  • Dubois F, Giraldeau L-A, Grant JWA (2003) Resource defense in a group-foraging context. Behav Ecol 14:2–9

    Google Scholar 

  • Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology, 3rd edn. Blackwell, Oxford, pp 301–337

    Google Scholar 

  • Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Festa-Bianchet M, Jorgenson JT, Berube CH, Portier C, Wishart WD (1997) Body mass and survival of bighorn sheep. Can J Zool 75:1372–1379

    Google Scholar 

  • Festa-Bianchet M, Gaillard J-M, Jorgenson JT (1998) Mass- and density-dependent reproductive success and reproductive costs in a capital breeder. Am Nat 152:367–379

    PubMed  CAS  Google Scholar 

  • Frank SA (1998) Foundations of social evolution. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Freund RJ, Littell RC (1991) SAS system for regression. SAS Institute, Cary, NC

    Google Scholar 

  • Giraldeau L-A (1988) The stable group and the determinants of foraging group size. In: Slobodchikoff CN (ed) The ecology of social behavior. Academic, New York, pp 33–53

    Google Scholar 

  • Giraldeau L-A, Beauchamp G (1999) Food exploition: searching for the optimal joining policy. Trends Ecol Evol 14:102–106

    PubMed  Google Scholar 

  • Giraldeau L-A, Caraco T (2000) Social foraging theory. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Gendreau Y, Cote SD, Festa-Bianchet M (2005) Maternal effects on post-weaning physical and social development in juvenile mountain goats (Oreamnos americanus). Behav Ecol Sociobiol 58:224–237

    Google Scholar 

  • Gompper MR, Gittleman JL, Wayne RK (1998) Dispersal, philopatry, and genetic relatedness in a social carnivore: comparing males and females. Mol Ecol 7:157–163

    PubMed  CAS  Google Scholar 

  • Goodwin GG, Greenhall AM (1961) A review of the bats of Trinidad and Tobago. Bull Am Mus Nat Hist 233:190–301

    Google Scholar 

  • Gopukumar N, Nathan RT, Doss PS, Prakash A, Emmanuel K, Balasingh J, Marimuthu G, Kunz TH (2003) Early ontogeny of foraging behaviour in the short-nosed fruit bat Cynopterus sphinx (Megachiroptera): preliminary results. Mammalia 67:139–145

    Article  Google Scholar 

  • Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, IL, pp 454–471

    Google Scholar 

  • Greenhall AM (1965) Sapucaia nut dispersal by greater spear-nosed bats in Trinidad. Caribb J Science 5:167–171

    Google Scholar 

  • Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21

    Google Scholar 

  • Hamilton WD (1964a) The genetical evolution of social behaviour, I. J Theor Biol 7:1–16

    PubMed  CAS  Google Scholar 

  • Hamilton WD (1964b) The genetical evolution of social behaviour, II. J Theor Biol 7:17–52

    PubMed  CAS  Google Scholar 

  • Heideman PD (1995) Synchrony and seasonality of reproduction in tropical bats. Symp Zool Soc Lond 67:151–165

    Google Scholar 

  • Higashi M, Yamamura N (1993) What determines animal group size? Insider–outsider conflict and its resolution. Am Nat 142:553–563

    Google Scholar 

  • Howell DJ (1979) Flock foraging in nectar-feeding bats: advantages to the bats and to the host plants. Am Nat 114:23–49

    Google Scholar 

  • Jerome CA, McInnes DA, Adams ES (1998) Group defense by colony-founding queens in the fire ant Solenopsis invicta. Behav Ecol 9:301–308

    Google Scholar 

  • Johnson DDP, Kays R, Blackwell PG, Macdonald DW (2002) Does the resource dispersion hypothesis explain group living? Trends Ecol Evol 17:563–570

    Google Scholar 

  • Kerth G, Wagner M, König B (2001) Roosting together, foraging apart: information transfer about food is unlikely to explain sociality in female Bechstein’s bats (Myotis bechsteini). Behav Ecol Sociobiol 50:283–291

    Google Scholar 

  • 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 52:203–210

    Google Scholar 

  • Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261

    PubMed  CAS  Google Scholar 

  • Kunz TH, Stern AA (1995) Maternal investment and post-natal growth in bats. In: Racey PA, Swift SM (eds) Ecology, evolution and behaviour of bats. Symposium of the Zoological Society of London, Oxford, pp 123–138

    Google Scholar 

  • Kutsukake N, Clutton-Brock T (2006) Aggression and submission reflect reproductive conflict between females in cooperatively breeding meerkats Suricata suricatta. Behav Ecol Sociobiol 59:541–548

    Google Scholar 

  • Laland KN, Richerson PJ, Boyd R (1996) Developing a theory of animal social learning. In: Heyes CM, Galef BG (eds) Social learning in animals: the roots of culture. Academic, New York, pp 129–155

    Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Google Scholar 

  • Larsson K, Forslund P (1992) Genetic and social inheritance of body and egg size in the barnacle goose (Branta leucopsis). Evolution 46:235–244

    Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Loison A, Langvatn R, Solberg EJ (1999) Body mass and winter mortality in red deer calves: disentangling sex and climate effects. Ecography 22:20–30

    Google Scholar 

  • McCracken GF (1987) Genetic structure of bat social groups. In: Racey PA, Fenton MB, Rayner JM (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 281–298

    Google Scholar 

  • McCracken GF, Bradbury JW (1977) Paternity and genetic heterogeneity in the polygynous bat, Phyllostomus hastatus. Science 198:303–306

    PubMed  Google Scholar 

  • McCracken GF, Bradbury JW (1981) Social organization and kinship in the polygynous bat Phyllostomus hastatus. Behav Ecol Sociobiol 8:11–34

    Google Scholar 

  • Mitchell-Olds T, Shaw R (1987) Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41:1149–1161

    Google Scholar 

  • Moore AJ, Boake CRB (1994) Optimality and evolutionary genetics: complementary procedures for evolutionary analysis in behavioural ecology. Trends Ecol Evol 9:69–72

    Google Scholar 

  • Packer C, Scheel D, Pusey AE (1990) Why lions form groups: food is not enough. Am Nat 136:1–119

    Google Scholar 

  • Petraitis PS, Dunham AE, Niewiarowski PH (1996) Inferring multiple causality: the limitations of path analysis. Funct Ecol 10:421–431

    Google Scholar 

  • Phillips PC, Arnold SJ (1989) Visualizing multivariate selection. Evolution 43:1209–1222

    Google Scholar 

  • Porter TA, Wilkinson GS (2001) Birth synchrony in greater spear-nosed bats. J Zool 253:383–390

    Google Scholar 

  • Potti J, Davila JA, Tella JL, Frias O, Villar S (2002) Gender and viability selection on morphology in fledgling pied flycatchers. Mol Ecol 11:1317–1326

    PubMed  CAS  Google Scholar 

  • Price TD (1998) Maternal and paternal effects in birds. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, Oxford, pp 202–226

    Google Scholar 

  • Price TD, Grant PR (1985) The evolution of ontogeny in Darwin’s finches: a quantitative genetic approach. Am Nat 125:169–188

    Google Scholar 

  • Ransome RD (1995) Earlier breeding shortens life in female greater horseshoe bats. Philos Trans R Soc Lond B 350:153–161

    Google Scholar 

  • Ranta E, Rita H, Lindstrom K (1993) Competition versus cooperation: success of individuals foraging alone and in groups. Am Nat 142:42–58

    CAS  PubMed  Google Scholar 

  • Reeve HK, Keller L (1996) Relatedness asymmetry and reproductive sharing in animal societies. Am Nat 148:764–769

    Google Scholar 

  • Rood JP (1990) Group size, survival, reproduction, and routes to breeding in dwarf mongooses. Anim Behav 39:566–572

    Google Scholar 

  • Rossiter SJ, Jones G, Ransome RD, Barratt EM (2002) Relatedness structure and kin-biased foraging in the greater horseshoe bat (Rhonolophus ferrumequinum). Behav Ecol Sociobiol 41:510–518

    Google Scholar 

  • Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79:135–160

    PubMed  Google Scholar 

  • Schluter D, Gustafsson L (1993) Maternal inheritance of condition and clutch size in the collared flycatcher. Evolution 47:658–667

    Google Scholar 

  • Schmidt-French B, Whitaker JO (2005) Acquisition of foraging behavior and insect preferences by naive juvenile red bats (Lasiurus borealis). Acta Chiropt 7:314–318

    Google Scholar 

  • Schneider KJ (1984) Dominance, predation, and optimal foraging in white-throated sparrow flocks. Ecology 65:1820–1827

    Google Scholar 

  • Sherman PW, Jarvis JUM, Alexander RD (1991) The biology of the naked mole-rat. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Sibly RH, Nott HMR, Fletcher DJ (1990) Splitting behaviour into bouts. Anim Behav 39:63–69

    Google Scholar 

  • Sibly RM (1983) Optimal group size is unstable. Anim Behav 31:946–951

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. Freeman, New York, NY

    Google Scholar 

  • Spiller DA (1992) Relationship between prey consumption and colony size in an orb spider. Oecologia 90:457–466

    Google Scholar 

  • Spong G, Stone J, Creel S, Bjorklund M (2002) Genetic structure of lions (Panthera leo) in the Selous Game Reserve: implications for the evolution of sociality. J Evol Biol 15:945–953

    Google Scholar 

  • Stacey PB, Koenig WD (1990) Cooperative breeding in birds. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Sterck, EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Google Scholar 

  • Stern AA (1996) Growth and reproductive energetics of the greater spear-nosed bat, Phyllostomus hastatus. Ph.D. thesis, Boston University, Boston, MA

  • Stern AA, Kunz TH, Studier EH, Oftedal OT (1997) Milk composition and lactational output in the greater spear-nosed bat, Phyllostomus hastatus. J Comp Physiol [B] 167:389–398

    CAS  Google Scholar 

  • Vucetich JA, Peterson RO, Waite TA (2004) Raven scavenging favours group foraging in wolves. Anim Behav 67:1117–1126

    Google Scholar 

  • Wade MJ, Kalisz S (1990) The causes of natural selection. Evolution 44:1947–1955

    Google Scholar 

  • West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296:72–75

    PubMed  CAS  Google Scholar 

  • White GC, Garrott RA, Bartmann RM, Carpenter LH, Alldredge AW (1987) Survival of mule deer in northwest Colorado. J Wildl Manage 51:852–859

    Google Scholar 

  • Wilkinson GS, Boughman JW (1998) Social calls coordinate foraging in greater spear-nosed bats. Anim Behav 55:337–350

    PubMed  Google Scholar 

  • Wilkinson GS, Boughman JW (1999) Social influences on foraging in bats. In: Box HO, Gibson KR (eds) Mammalian social learning: comparative and ecological perspectives. Cambridge University Press, Cambridge, pp 188–204

    Google Scholar 

  • Wolf JB (2003) Genetic architecture and evolutionary constraint when the environment contains genes. Proc Natl Acad Sci USA 100:4655–4660

    PubMed  CAS  Google Scholar 

  • Woolfenden GE, Fitzpatrick JW (1990) Florida scrub jays: a synopsis after 18 years of study. In: Stacey PB, Koenig WD (eds) Cooperative breeding in birds. Cambridge University Press, Cambridge, pp 239–266

    Google Scholar 

  • Wrangham RW (1982) Mutualism, kinship and social evolution. In: Kings College Sociobiology Group (eds) Current problems in sociobiology. Cambridge University Press, Cambridge, pp 269–289

    Google Scholar 

Download references

Acknowledgements

The able assistance of Skye Boughman, Sue Perkins, Traci Porter, Baldeo Ramlal, Jerry Wilkinson, and Jason Wolf made collection of data possible. Traci Porter and April Stern generously shared banding data. I thank Felix Breden, Dov Lank, Dolph Schluter, and Jamie Smith for discussion that clarified some of the ideas presented here. Luc-Alain Giraldeau, Daven Presgraves, Dolph Schluter, Jamie Smith, David Westneat, Jerry Wilkinson, and three anonymous reviewers provided comments that greatly improved the manuscript. Financial assistance was provided by the Smithsonian Institution, the National Science Foundation, Sigma Xi, American Museum of Natural History, American Women in Science, American Society of Mammalogists, and Eugenie Clark Research Fund. Additional support was provided by a NSF grant to GS Wilkinson. This work was conducted in accordance with animal care regulations at the University of Maryland.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Janette Wenrick Boughman.

Additional information

Communicated by T. Czeschlik

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boughman, J.W. Selection on social traits in greater spear-nosed bats, Phyllostomus hastatus . Behav Ecol Sociobiol 60, 766–777 (2006). https://doi.org/10.1007/s00265-006-0220-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0220-2

Keywords

Navigation