Skip to main content
SpringerLink
Log in

Extreme polygyny in the previously unstudied subtropical ant Temnothorax tuscaloosae with implications for the biogeographic study of the evolution of polygyny

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Evolutionary ecologists often seek to explain life history variation at geographical scales. Progress in this regard has been slower in social insects than in unitary organisms, due in part to limited information about species distributions and the complexity of studying colony-level traits. Temnothorax ants have proven useful for investigating associations between ecology and life history traits in ants, because they have small colonies (<200 workers) with substantial variation in traits like queen number within and across populations. Yet most of these studies have focused on <10 Temnothorax species from northern latitudes, although the genus contains >400 species that range from temperate to tropical biomes. Here, we generate the first global map of Temnothorax diversity and demonstrate that previous ecological hypotheses for colony life history variation in the genus are based on data and studies confined to a small part of the overall genus-level distribution. For example, studies of northern-latitude species have suggested that overwintering success is a prominent selective force favoring polygyny but little is known about polygyny in Temnothorax species from other regions. We report the highest observed queen numbers known in the genus in the subtropical species T. tuscaloosae and confirm that all queens in these polygynous colonies are mated and actively laying eggs. Behavioral laboratory experiments further indicate that this species has a fluid nest structure and lacks intraspecific aggression at the whole-forest scale. These results extend the biogeographical extent of life history studies for this genus and point to evolutionary discoveries awaiting comparative research of the global Temnothorax fauna.

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

Access this article

Log in via an institution

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

  • Alloway TM, Buschinger A, Talbot M, Stuart R, Thomas C (1982) Polygyny and polydomy in three North American species of the genus Leptothorax Mayr (Hymenoptera: Formicidae). Psyche 89:249–274

    Article  Google Scholar 

  • Antcat.org (2016) http://www.antcat.org/. Accessed 7 Jan 2016

  • Antmaps.org (2015) http://www.antmaps.org/. Accessed 30 Dec 2015

  • Bengston SE, Dornhaus A (2014) Be meek or be bold? A colony-level behavioural syndrome in ants. Proc R Soc B 281:20140518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257

    Article  Google Scholar 

  • Bourke AF, Heinze J (1994) The ecology of communal breeding: the case of multiple-queen leptothoracine ants. Phil Trans R Soc B 345:359–372

    Article  Google Scholar 

  • Brown WL Jr, Wilson EO (1956) Character displacement. Syst Zool 5:49–64

    Article  Google Scholar 

  • Brown JH, Marquet PA, Taper ML (1993) Evolution of body size: consequences of an energetic definition of fitness. Am Nat 142:573–584

    Article  CAS  PubMed  Google Scholar 

  • Buschinger A, Alloway TM (1978) Caste polymorphism in Harpaxogenus canadensis M.R. Smith (Hym., Formicidae). Insectes Soc 25:339–350

    Article  Google Scholar 

  • Carter WG (1962) Ant distribution in North Carolina. J Elisha Mitchell Sci Soc 78:150–204

    Google Scholar 

  • Csősz S, Seifert B, Müller B, Trindl A, Schulz A, Heinze J (2014) Cryptic diversity in the Mediterranean Temnothorax lichtensteini species complex (Hymenoptera: Formicidae). Org Divers Evol 14:75–88

    Article  Google Scholar 

  • Csősz S, Heinze J, Mikó I (2015) Taxonomic synopsis of the Ponto-Mediterranean ants of Temnothorax nylanderi species-group. PLoS One 10:e0140000. doi:10.1371/journal.pone.0140000

    Article  PubMed  PubMed Central  Google Scholar 

  • Debout G, Schatz B, Elias M, McKey D (2007) Polydomy in ants: what we know, what we think we know, and what remains to be done. Biol J Linnean Soc 90:319–348

    Article  Google Scholar 

  • Deyrup M (2003) An updated list of Florida ants (Hymenoptera: Formicidae). Fla Entomol 86:43–48

    Article  Google Scholar 

  • Deyrup M, Cover S (2004) A new species of the ant genus Leptothorax from Florida, with a key to the Leptothorax of the southeast (Hymenoptera: Formicidae). Fla Entomol 87:51–59

    Article  Google Scholar 

  • Ellison AM, Gotelli NJ, Farnsworth EJ, Alpert GD (2012) A field guide to the ants of New England. Yale University Press, New Haven

    Google Scholar 

  • Evans JD, Pierce NE (1995) Effects of diet quality and queen number on growth in Leptothoracine ant colonies (Hymenoptera: Formicidae). J N Y Entomol Soc 103:91–99

    Google Scholar 

  • Foitzik S, Heinze J (1998) Nest site limitation and colony takeover in the ant Leptothorax nylanderi. Behav Ecol 9:367–375

    Article  Google Scholar 

  • Foitzik S, Backus VL, Trindl A, Herbers JM (2004) Ecology of Leptothorax ants: impact of food, nest sites, and social parasites. Behav Ecol Sociobiol 55:484–493

    Article  Google Scholar 

  • Guénard B, Weiser MD, Dunn RR (2012a) Global models of ant diversity suggest regions where new discoveries are most likely are under disproportionate deforestation threat. Proc Natl Acad Sci USA 109:7368–7373

    Article  PubMed  PubMed Central  Google Scholar 

  • Guénard B, McCaffrey KA, Lucky A, Dunn RR (2012b) Ants of North Carolina: an updated list (Hymenoptera: Formicidae). Zootaxa 3552:1–36

    Google Scholar 

  • Headley AE (1943) Population studies of two species of ants, Leptothorax longispinosus Roger and Leptothorax curvispinosus Mayr. Ann Entomol Soc Am 36:743–753

    Article  Google Scholar 

  • Heinze J (2006) Life in a nutshell—social evolution in formicoxenine ants. In: Kipyatkov VE (ed) Life cycles in social insects: behaviour, ecology and evolution. Petersburg University Press, St. Petersburg, pp 49–61

    Google Scholar 

  • Heinze J, Buschinger A (1988) Polygyny and functional monogyny in Leptothorax ants (Hymenoptera: Formicidae). Psyche 95:309–326

    Article  Google Scholar 

  • Heinze J, Rueppell O (2014) The frequency of multi-queen colonies increases with altitude in a Nearctic ant. Ecol Entomol 39:527–529

    Article  Google Scholar 

  • Heinze J, Foitzik S, Hippert A, Hölldobler B (1996) Apparent dear-enemy phenomenon and environment-based recognition cues in the ant Leptothorax nylanderi. Ethology 102:510–522

    Article  Google Scholar 

  • Herbers JM (1984) Queen-worker conflict and eusocial evolution in a polygynous ant species. Evolution 38:631–643

    Article  Google Scholar 

  • Herbers JM (1986a) Effects of ecological parameters on queen number in Leptothorax longispinosus (Hymenoptera; Formicidae). J Kans Entomol Soc 59:675–686

    Google Scholar 

  • Herbers JM (1986b) Nest site limitation and facultative polygyny in the ant Leptothorax longispinosus. Behav Ecol Sociobiol 19:115–122

    Article  Google Scholar 

  • Herbers JM (1993) Ecological determinants of queen number in ants. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, New York, pp 262–293

    Google Scholar 

  • Herbers JM, Johnson CA (2007) Social structure and winter survival in acorn ants. Oikos 116:829–835

    Article  Google Scholar 

  • Herbers JM, Stuart RJ (1996) Patterns of reproduction in Southern versus Northern populations of Leptothorax ants (Hymenoptera: Formicidae). Ann Entomol Soc Am 89:354–360

    Article  Google Scholar 

  • Herbers JM, Tucker CW (1986) Population fluidity in Leptothorax longispinosus (Hymenoptera; Formicidae). Psyche 93:217–229

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1977) The number of queens: an important trait in ant evolution. Naturwissenschaften 64:8–15

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (2008) The Superorganism: the beauty, elegance, and strangeness of insect societies. W. W. Norton and Company, New York

    Google Scholar 

  • Hou C, Kaspari M, Vender Zanden HB, Gillooly JF (2010) Energetic basis of colonial living in social insects. Proc Natl Acad Sci USA 107:3634–3638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes WHO, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216

    Article  CAS  PubMed  Google Scholar 

  • James FC (1970) Geographic size variation in birds and its relationship to climate. Ecology 51:365–390

    Article  Google Scholar 

  • Janicki JH, Narula N, Ziegler M, Guénard B, Economo EP (2016) Visualizing and interacting with large-volume biodiversity data using client-server web mapping applications: the design and implementation of antmaps.org. Ecol Inform 32:185–193

    Article  Google Scholar 

  • Johnson CA, Herbers JM (2006) Impact of parasite sympatry on the geographic mosaic of coevolution. Ecology 87:382–394

    Article  PubMed  Google Scholar 

  • Kaspari M (2005) Global energy gradients and the regulation of body size: worker mass and worker number in ant colonies. Proc Natl Acad Sci USA 102:5079–5083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 145:610–632

    Article  Google Scholar 

  • Kaspari M, Ward PS, Yuan M (2004) Energy gradients and the geographic distribution of local ant diversity. Oecologia 140:407–414

    Article  PubMed  Google Scholar 

  • Kikuchi T, Tsuji K, Ohnishi H, Le Breton J (2007) Caste-biased acceptance of non-nestmates in a polygynous ponerine ant. Anim Behav 73:559–565

    Article  Google Scholar 

  • Lack DL (1947) The significance of clutch size, parts 1 and 2. Ibis 89:302–352

    Article  Google Scholar 

  • Lessard JP, Borregaard MK, Fordyce JA, Rahbek C, Weiser MD, Dunn RR, Sanders NJ (2012) Strong influence of regional species pools on continent-wide structuring of local communities. Proc R Soc B 279:266–274

    Article  PubMed  Google Scholar 

  • Linksvayer TA (2008) Queen-worker-brood coadaptation rather than conflict may drive colony resource allocation in the ant Temnothorax curvispinosus. Behav Ecol Sociobiol 62:647–657

    Article  Google Scholar 

  • Lubertazzi D, Alpert GD (2014) The ants (Hymenoptera: Formicidae) of Jaragua National Park. J Insects. Article ID 104157:6 pages. doi:10.1155/2014/104157

  • MacGown JA (2006) Hickory nuts used as nesting sites by ants (Hymenoptera: Formicidae). Marginalia Insecta 1:1–3

    Google Scholar 

  • MacGown JA, Brown RL (2006) Survey of ants (Hymenoptera: Formicidae) of the Tombigbee National Forest in Mississippi. J Kans Entomol Soc 79:325–340

    Article  Google Scholar 

  • MacGown JA, Forster JA (2005) A preliminary list of the ants (Hymenoptera: Formicidae) of Alabama, USA. Entomol News 116:61–74

    Google Scholar 

  • NOAA.gov (2016), National Oceanic and Atmospheric Administration, National Centers for Environmental Information. http://www.ncdc.noaa.gov/. Accessed 16 June 2016

  • Nonacs P, Kapheim KM (2010) Social heterosis and the maintenance of genetic diversity. J Evol Biol 20:2253–2265

    Article  Google Scholar 

  • Peeters C (1993) Monogyny and polygyny in ponerine ants with or without queens. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, Oxford, pp 234–261

    Google Scholar 

  • Prebus M (2015) Palearctic elements in the old world tropics: a taxonomic revision of the ant genus Temnothorax Mayr (Hymenoptera, Formicidae) for the Afrotropical biogeographical region. Zookeys 483:23–57

    Article  PubMed  Google Scholar 

  • Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171

    Article  CAS  PubMed  Google Scholar 

  • Rüppell O, Heinze J, Hölldobler B (1998) Size-dimorphism in the queens of the North American ant Leptothorax rugatulus (Emery). Insectes Soc 45:67–77

    Article  Google Scholar 

  • Rüppell O, Heinze J, Hölldobler B (2001a) Alternative reproductive tactics in the queen-size-dimorphic ant Leptothorax rugatulus (Emery) and their consequences for genetic population structure. Behav Ecol Sociobiol 50:189–197

    Article  Google Scholar 

  • Rüppell O, Heinze J, Hölldobler B (2001b) Genetic and social structure of the queen size dimorphic ant Leptothorax cf. andrei. Ecol Entomol 26:76–82

    Article  Google Scholar 

  • Salata S, Borowiec L (2015) Redescription of Temnothorax antigoni (Forel, 1911) and description of its new social parasite Temnothorax curtisetosus sp. n. from Turkey (Hymenoptera, Formicidae). ZooKeys 523:129–148

    Article  PubMed  Google Scholar 

  • Sanders NJ, Gotelli NJ, Heller NE, Gordon DM (2003) Community disassembly by an invasive species. Proc Natl Acad Sci USA 100:2474–2477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos JC, Cannatella DC (2011) Phenotypic integration emerges from aposematism and scale in poison frogs. Proc Natl Acad Sci USA 108:6175–6180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seifert B, Csösz S (2015) Temnothorax crasecundus sp. n.—a cryptic Eurocaucasian ant species (Hymenoptera, Formicidae) discovered by Nest Centroid Clustering. ZooKeys 479:37–64

    Article  PubMed  Google Scholar 

  • Shik JZ (2008) Ant colony size and the scaling of reproductive effort. Funct Ecol 22:674–681

    Article  Google Scholar 

  • Shik JZ, Hou C, Kay A, Kaspari M, Gillooly JF (2012) Toward a general life history model of the superorganism: predicting the survival, growth, and reproduction of ant societies. Biol Lett 8:1059–1062

    Article  PubMed  PubMed Central  Google Scholar 

  • Stuart RJ (1985) Spontaneous polydomy in laboratory colonies of the ant Leptothorax curvispinosus Mayr (Hymenoptera: Formicidae). Psyche 92:71–82

    Article  Google Scholar 

  • Stuart RJ (1992) Nestmate recognition and the ontogeny of acceptability in the ant, Leptothorax curvispinosus. Behav Ecol Sociobiol 30:403–408

    Article  Google Scholar 

  • Stuart RJ, Gresham-Bissett L, Alloway TM (1993) Queen adoption in the polygynous and polydomous ant, Leptothorax curvispinosus. Behav Ecol 4:276–281

    Article  Google Scholar 

  • Talbot M (1957) Population studies of the slave-making ant Leptothorax duloticus and its slave, Leptothorax curvispinosus. Ecology 38:449–456

    Article  Google Scholar 

  • Tschinkel WR (2011) Back to basics: sociometry and sociogenesis of ant societies (Hymenoptera: Formicidae). Myrmecol News 14:49–54

    Google Scholar 

  • Tsuji K (2010) What brings peace to the world of ants (Hymenoptera: Formicidae)? Myrmecol News 13:131–132

    Google Scholar 

  • Ugelvig LV, Kronauer DJC, Schrempf A, Heinze J, Cremer S (2010) Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc R Soc B 277:2821–2828

    Article  PubMed  PubMed Central  Google Scholar 

  • Ward PS, Brady SG, Fisher BL, Schultz TR (2015) The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae). Syst Entomol 40:61–81. doi:10.1111/syen.12090

    Article  Google Scholar 

  • Wheeler WM (1931) New and little-known ants of the genera Macromischa, Creosomyrmex and Antillaemyrmex. Bull Mus Comp Zool 72:1–34

    Google Scholar 

  • Wilson EO (1951) A new Leptothorax from Alabama (Hymenoptera: Formicidae). Psyche 57:128–130

    Article  Google Scholar 

Download references

Acknowledgments

We dedicate this paper to E. O. Wilson who described T. tuscaloosae in 1951 in his first taxonomic paper on ants. We would like to thank Tim Linksvayer and Joe MacGown for providing us records, respectively, from Tennessee and Mississippi. Collections in State Parks of North Carolina were supported by a permit from the NC Division of Parks and Recreation. Collections in Georgia National Forests were supported by a permit from the US Forest Service. Collections conducted in Virginia, West Virginia and Lake Raleigh (NC) were performed on private lands with permission from their respective owners. Ed Olson and John Blake for their assistance in locating field sites at Savannah River Site, a National Environmental Research Park. Logistical support was provided by the Department of Energy-Savannah River Operations Office through the U.S. Forest Service Savannah River under Interagency Agreement DE-AI09-00SR22188. Mike Joyce and the U.S. Forest service for permitting research insect collections.

Author information

Author notes

    Authors and Affiliations

    1. School of Biological Sciences, University of Hong Kong, Pok Fu Lam, Hong Kong

      B. Guénard

    2. Smithsonian Tropical Research Institute, Balboa, Republic of Panama

      J. Z. Shik

    3. Department of Biology, Centre for Social Evolution, University of Copenhagen, Universitetsparken 15, 2100, Copenhagen, Denmark

      J. Z. Shik

    4. Department of Ecology and Evolutionary Biology, University of California Los Angeles, 621 Charles E. Young Drive S, Los Angeles, CA, 90095-1606, USA

      D. Booher

    5. Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA

      D. Lubertazzi & G. Alpert

    Authors
    1. B. Guénard
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. J. Z. Shik
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. D. Booher
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. D. Lubertazzi
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. G. Alpert
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to B. Guénard.

    Additional information

    B. Guénard and J. Z. Shik with equal contributions to the study.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 34001 kb)

    Supplementary material 2 (XLSX 47 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Guénard, B., Shik, J.Z., Booher, D. et al. Extreme polygyny in the previously unstudied subtropical ant Temnothorax tuscaloosae with implications for the biogeographic study of the evolution of polygyny. Insect. Soc. 63, 543–551 (2016). https://doi.org/10.1007/s00040-016-0498-7

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00040-016-0498-7

    Keywords

    Search

    Navigation