1. Ecology
  2. Evolutionary Biology
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Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors

  1. Roberto A Keller  Is a corresponding author
  2. Christian Peeters
  3. Patrícia Beldade
  1. Instituto Gulbenkian de Ciência, Portugal
  2. CNRS UMR 7625, Université Pierre et Marie Curie, France
Research Article
Cite this article as: eLife 2014;3:e01539 doi: 10.7554/eLife.01539
3 figures, 3 tables and 1 data set


Figure 1 with 2 supplements
Variation in length of first (T1) and second (T2) thoracic segments in ants shows characteristic differences depending on caste and species.

(A) Relative lengths of T1 and T2 (left) show clear differences between queens and workers for 11 ant species. T3 (right) constitutes a small portion of the total length of the thorax in both queens and workers and, when present (when T3/TL > 0.0), is indistinguishable between castes. Numbers correspond to sample sizes and are equal for both panels (Table 1). (B) Gradient of investment in neck strength vs flight/storage musculature sorts individuals into three categories. Queens fall into two discrete categories based on the relative lengths of T1 and T2. While the use of T1/T2 in (A) emphasizes the distinction between workers and queens and within species variation, T1/TL and T2/TL in (B) enables the distinction between queen types across species with large differences in body size. Measurements and ratios are available in the Dryad data repository under DOI doi: 10.5061/dryad.d62p2/1 (Keller et al., 2014). Species codes: A. aus = Amblyopone australis; B. lut = Brachyponera lutea; C. vid = Carebara vidua; C. was = Cataulacus wasmanni; L. nig = Lasius niger; L. per = Leptothorax pergandei; M. pha = Monomorium pharaonis; N. api = Neoponera apicalis; P. bar = Pogonomyrmex barbatus; P. lab = Polyrhachis laboriosa; T. aet = Tetraponera aethiops.

Figure 1—figure supplement 1
Measurements used in this study.

The length of the first (T1 = pronotum), second (T2 = mesonotum) and third (T3 = metanotum) dorsal thoracic plates was measured along the dorsal midline. Total thoracic length (TL) was measured as the diagonal length in profile from the anterior-most point of the first thoracic segment to the posterior-most point of the third thoracic segment (also known as Weber's length). For each of the specimens measured, images of dorsal and profile views are available in the Dryad data repository under DOI doi: 10.5061/dryad.d62p2/2. Note that the total length of the thorax (TL) is always greater than the sum of the lengths of the dorsal thoracic plates (T1 to T3), because in ants (as in most Hymenoptera) the first abdominal segment (A1 = propodeum) is fused dorsally to the thorax and occupies most of the posterior part of the mesosomal region. A2 = second abdominal segment. Scale bars = 1.0 mm.

Figure 1—figure supplement 2
Differences in length proportion of thoracic segments among castes in nine representative species from different subfamilies.

T2 is always larger than T1 in queens (top), while T1 is larger than T2 in workers (bottom). (A) Aneuretus simoni (Aneuretinae); (B) Discothyrea testacea (Proceratiinae); (C) Ectatomma tuberculatum (Ectatomminae); (D) Myopopone castanea (Amblyoponinae); (E) Myrmecia chasei (Myrmeciinae); (F) Myrmica emeryana (Myrmicinae); (G) Pseudoponera stigma (Ponerinae); (H) Pseudomyrmex gracilis (Pseudomymecinae); (I) Tapinoma erraticum (Dolichoderinae). White-black-white on thick bars equals length of T1, T2, and T3 respectively. Note that T3 has no distinguishable dorsum in workers of most species. Scale bars upper left, 1 mm. All images by April Nobile/antweb.org.

Figure 2 with 2 supplements
Skeletomuscular specialization of queens and workers in ants.

The dorsal plate of T1 is always enlarged in workers relative to queens (left column; multiple individuals from 52 genera examined, Table 2). Queens can either (A) have a reduced T1 and huge T2-associated wing muscles (represented here by Oecophylla smaragdina), or (B) show a slightly enlarged T1 and associated neck muscles (represented here by Neoponera apicalis). T1, T2, and T3, first, second and third thoracic segments respectively; A1, first abdominal segment. Workers of N. apicalis lack a discernible T3. Internally (right column), the wing muscles in queens (red) fill most of the thoracic cavity, while the T1 muscles (blue) are narrow and close to the thoracic wall. In all workers examined (see Table 1 for list of species and sample sizes), the T1 notopleural muscles (np, dark blue) that support the anteroventral plates (yellow) fill the anterior portion of the cavity. The dorsal cervical muscles (dc, light blue; see also Figure 2—figure supplement 1B) that in winged queens originate at the anterior phragma and pull the head up at contraction, show a shifted position in workers. In the absence of phragma, these muscles originate at the dorsal boundary between T1 and T2. Rather than being short and thin, they form long and thick bundles that stretch the entire length of the enlarged T1 cavity to their place of insertion on the back of the head (Figure 2—figure supplement 2). Figure 1—supplement 1 has photos of many more species of ‘reduced T1’ and ‘intermediate T1’ species for comparison of external thoracic morphology.

Figure 2—figure supplement 1
Thoracic musculature in queen and worker ants.

(A) Sagittal section of a queen (Polyrhachis laboriosa) reveals the thoracic cavity filled by the longitudinal (lw) and dorsoventral (dw) indirect wing-muscles (he, head; T1, pronotum; T2, mesonotum; T3 metanotum; A1, first abdominal segment; A2, second abdominal segment; ap, anterior phragma). (B) Anterior view of the queen's T2 shows the thin dorsal cervical muscle pair (dc) that originates at the anterior phragma (ap). (C) Removing the wing muscles and the dorsal plates of T1 and T2 exposes the notopleural muscle pair (np) inside the anterior part of the thorax (left column is dorsal view, right column is profile view; tissues are stained with methylene blue). These muscles are thin and narrow in queens (first row P. laboriosa, second row Neoponera apicalis). Equivalent muscles in ant workers are hypertrophied, and fill the T1 cavity completely (third row, N. apicalis). Scale bar = 1 mm.

Figure 2—figure supplement 2
Internal anatomical adaptations in ant workers for powerful head movement.

(A) One dorsal pair of prothoracic muscles (dc, dorsal cervical) traverses the enlarged workers' T1 cavity and pulls the head up at contraction; the expanded prothoracic endosternum (pe) is the origin for two pairs of muscles (dorsal and ventral) that move the head up-and-down. (B) Skeletal preparations of 18 species (Table 1) revealed that workers show enlargement of the endosternum, an internal skeletal structure that branches inside T1 for attachment of muscles that, in bees, power up-and-down movement of the head (left column is profile view, right column is frontal view; represented by Neoponera apicalis; scale bar, 500 µm). While in queens, the T1 endosternum has an upper face (up) perpendicular to its basal stalk (ba), in workers the upper face rises almost parallel to the basal stalk and has a larger surface for the attachment of the muscles that pull the head. This modification of the endosternum in workers is only possible because the complete absence of wing muscles that occur in this caste leaves the thoracic cavity with sufficient space for the expansion of T1 internal structures. In queens (as is the case in all castes of honey bees), the perpendicular orientation of the endosternal face is necessary for the occurrence of the longitudinal wing muscles across the thoracic cavity.

Phylogenetic reconstruction reveals a single origin of a hypertrophied T1 in workers and multiple independent origins of ‘reduced’ T1 in queens.

The latter is associated with modifications in modes of colony foundation. Tree branches and tree background are colored for queen morphology and founding behavior respectively, according to the parsimony ancestral reconstruction. Typical queen-worker dimorphism shown to the right to illustrate ratio T1/T2 (not to scale). Species with wingless queens are marked with an asterisk. Phylogeny was pruned from Moreau et al. (2006). Placement of Sphecomyrma and Martialis after Grimaldi et al. (1997) and Rabeling et al. (2008), respectively. Metapolybia and Scolia wasps are included as outgroups. Data on the species are analyzed, and their morphology and type of colony founding behavior are summarized in Table 3. Numbers correspond to major taxonomic groups within Formicidae after Ward (2007): 1, Sphecomyrminae; 2, Leptanillinae; 3, Martialinae; 4, Proceratiinae; 5, Amblyoponinae; 6, Paraponerinae; 7, Agroecomyrmecinae; 8, Ponerinae; 9, dorylomorphs; 10, myrmeciomorphs; 11, dolichoderomorphs; 12, ectaheteromorphs; 13, Formicinae; 14, Myrmicinae.



Table 1

Ant species studied for morphometrics and/or internal anatomy

AmblyoponinaeAmblyopone australis6822
DolichoderinaeTapinoma simrothi610
EctatomminaeEctatomma ruidum35
FormicidaeLasius niger151524
Oecophylla smaragdina25
Polyrhachis laboriosa13538
MyrmeciinaeMyrmecia simillima24
Nothomyrmecia macrops14
MyrmicinaeCarebara vidua5311
Cataulacus wasmanni151533
Leptothorax pergandei131513
Messor barbarus38
Monomorium pharaonis151524
Monomorium subopacum23
Pogonomyrmex barbatus151745
PonerinaeBrachyponera lutea151535
Harpegnathos saltator24
Neoponera apicalis712410
PseudomyrmecinaeTetraponera aethiops111546
  1. q = number of queens examined; w = number of workers examined. Generic placement of Brachyponera lutea and Neoponera apicalis reflects the new reclassification of species within the former paraphyletic genus Pachycondyla (Schmidt CA, Shattuck SO, The higher classification of the ant subfamily Ponerinae [Hymenoptera: Formicidae], with a review of ponerine ecology and behavior. Under review).

Table 2

List of species surveyed for relative length of thoracic segments

MuseumVoucher codeMuseumVoucher code
 AenictinaeAenictus vaucheri/binghamiMSNGCASENT0903754AMNHRAK0094
 AgroecomyrmecinaeTatuidris tatusiaDADCCASENT0178881BMNHRAK0001
 AmblyoponinaeAdetomyrma spAMNHRAK0003
 AmblyoponinaeAmblyopone australisANICCASENT0172213AMNHRAK0005
 AmblyoponinaeAmblyopone mercovichiMCZRAK0006
 AmblyoponinaeApomyrma stygiaMNHNCASENT0101445MCZRAK0083
 AmblyoponinaeConcoctio concentaMCZRAK0011
 AmblyoponinaeMyopopone castaneaANICCASENT0172069AMNHRAK0012
 AmblyoponinaeMystrium spCASCCASENT0104559CASCCASENT0076622
 AmblyoponinaeOnychomyrmex doddiAMNHRAK0014
 AmblyoponinaePrionopelta punctulataANICCASENT0172312AMNHRAK0016
 AmblyoponinaeStigmatomma armigeraAMNHRAK0004
 AmblyoponinaeStigmatomma pallipesABSCASENT0103553MCZRAK0009
 AmblyoponinaeStigmatomma plutoMCZRAK0010
 AmblyoponinaeXymmer muticusMCZRAK0007
 AneuretinaeAneuretus simoniANICCASENT0172259MCZRAK0074
 CerapachyinaeAcanthostichus serratulusAMNHRAK0095
 CerapachyinaeCerapachys nitidulusRAKCRAK127AMNHRAK0096
 CerapachyinaeCerapachys doryloidesAMNHRAK0097
 CerapachyinaeCylindromyrmex brevitarsusJTLCCASENT0610653AMNHRAK0098
 CerapachyinaeSimopone schoutedeniAMNHRAK0099
 DolichoderinaeDolichoderus bispinosusALWCCASENT0173835ALWCCASENT0173833
 DolichoderinaeIridomyrmex lividusANICCASENT0172066ANICCASENT0172041
 DolichoderinaeLeptomyrmex pallensAMNHRAK0075
 DolichoderinaeTapinoma erraticumCASCCASENT0173200AMNHRAK0078
 DolichoderinaeTechnomyrmex albipesCASCCASENT0060419AMNHRAK0079
 DorylinaeDorylus conradti/helvolusMSNGCASENT0903712AMNHRAK0100
 EcitoninaeCheliomyrmex morosusAMNHRAK0101
 EcitoninaeEciton hamatumJTLCINBIOCRI001283500AMNHRAK0103
 EcitoninaeLabidus coecusAMNHRAK0102
 EctatomminaeEctatomma tuberculatumJTLCJTLC000014186AMNHRAK0017
 EctatomminaeGnamptogenys annulataAMNHRAK0018
 EctatomminaeGnamptogenys striatulaMIZACASENT0178660AMNHRAK0019
 EctatomminaeGnamptogenys bufonisMCZRAK0020
 EctatomminaeGnamptogenys minutaMCZRAK0021
 EctatomminaeRhytidoponera metallicaANICCASENT0172346ANICCASENT0172345
 EctatomminaeTyphlomyrmex pusillusMIZACASENT0178662AMNHRAK0023
 EctatomminaeTyphlomyrmex rogenhoferiAMNHRAK0024
 FormicinaeFormica sp. (fusca group)CASCCASENT0173171AMNHRAK0080
 FormicinaeLasius flavusCASCCASENT0173149UCDCCASENT0005406
 FormicinaeOecophylla smaragdinaCASCCASENT0173644AMNHRAK0082
 FormicinaePolyergus spRAKCRAK0129RAKCRAK0130
 FormicinaePolyrhachis revoiliCASCCASENT0403971CASCCASENT0227558
 HeteroponerinaeAcanthoponera minorAMNHRAK0025
 HeteroponerinaeHeteroponera brouniMCZRAK0128AMNHRAK0026
 HeteroponerinaeHeteroponera relictaAMNHRAK0027
 LeptanillinaeLeptanilla swaniAMNHRAK129AMNHRAK0084
 LeptanilloidinaeLeptanilloides erinys/biconstrictaUCDCCASENT0234616AMNHRAK0104
 MartialinaeMartialis heurekaMZSPCASENT0106181
 MyrmeciinaeMyrmecia gulosaCASCCASENT0103309CASCCASENT0103310
 MyrmeciinaeNothomyrmecia macropsAMNHRAK0086
 MyrmicinaeAphaenogaster fulvaCASCCASENT0104857CASCCASENT0103585
 MyrmicinaeCarebara viduaCASCCASENT0260121CASCCASENT0010803
 MyrmicinaeCataulacus wasmanniCASCCASENT0498338CASCCASENT0498558
 MyrmicinaeLeptothorax pergandeiMCZRAK0125MCZRAK0126
 MyrmicinaeManica rubidaAMNHRAK0090
 MyrmicinaeMessor barbarusRAKCRAK0123RAKCRAK0124
 MyrmicinaeMetapone madagascaricaCASCCASENT0004524MCZRAK0093
 MyrmicinaeMonomorium pharaonisABSCASENT0104094ABSCASENT0104095
 MyrmicinaeMyrmica wheeleriMCZCASENT0102860MCZCASENT0102862
 MyrmicinaePogonomyrmex uruguayensisRAJCCASENT0172689RAJCCASENT0103054
 ParaponerinaeParaponera clavataRAKCRAK0122AMNHRAK0028
 PonerinaeAnochetus mayriABSCASENT0103555MCZCASENT0003324
 PonerinaeAsphinctopone silvestriiMCZRAK0031
 PonerinaeBelonopelta deletrixMCZRAK0032
 PonerinaeBothroponera pachydermaAMNHRAK0054
 PonerinaeBrachyponera croceicornisAMNHRAK0051
 PonerinaeCentromyrmex brachycolaUCDCCASENT0178343AMNHRAK0033
 PonerinaeCryptopone gilvaCASCCASENT0006055AMNHRAK0034
 PonerinaeDiacamma ceylonenseAMNHRAK0035
 PonerinaeDinoponera lucidaAMNHRAK0036
 PonerinaeDolioponera fustigeraMCZRAK0037
 PonerinaeEmeryopone buttelreepeniMCZRAK0038
 PonerinaeHagensia marleyiMCZRAK0053
 PonerinaeHarpegnathos saltatorAMNHRAK0039
 PonerinaeHypoponera sp1.AMNHRAK0040
 PonerinaeLeptogenys (Leptogenys) sp.1AMNHRAK0041
 PonerinaeLeptogenys (Lobopelta) sp.2AMNHRAK0042
 PonerinaeLeptogenys podenzanaiMCZRAK0043
 PonerinaeLoboponera obeliscataAMNHRAK0044
 PonerinaeLoboponera vigilansAMNHRAK0045
 PonerinaeMyopias chapmaniANICCASENT0172094ANICCASENT0172093
 PonerinaeNeoponera apicalisALWCCASENT0103060AMNHRAK0048
 PonerinaeNeoponera villosaAMNHRAK0058
 PonerinaeOdontomachus bauriCASCCASENT0172630AMNHRAK0030
 PonerinaeOdontoponera transversaBMNHCASENT0900664AMNHRAK0047
 PonerinaeOphthalmopone berthoudiMCZRAK0049
 PonerinaePachycondyla crassinodaAMNHRAK0050
 PonerinaeCryptopone guianensisMCZRAK0052
 PonerinaePseudoneoponera porcataAMNHRAK0055
 PonerinaePseudoponera stigmaAMNHRAK0056
 PonerinaePaltothyreus tarsatusAMNHRAK0057
 PonerinaePhrynoponera gabonensisAMNHRAK0059
 PonerinaePlatythyrea punctataABSCASENT0104429AMNHRAK0060
 PonerinaePlatythyrea turneriMCZRAK0061
 PonerinaePlectroctena strigosaAMNHRAK0062
 PonerinaePonera alphaMCZRAK0063
 PonerinaePonera pennsylvanicaCASCCASENT0006086AMNHRAK0064
 PonerinaePsalidomyrmex procerusAMNHRAK0065
 PonerinaeSimopelta oculataMCZRAK0066
 PonerinaeStreblognathus peetersiAMNHRAK0067
 PonerinaeThaumatomyrmex atroxAMNHRAK0068
 ProceratiinaeDiscothyrea oculataAMNHRAK0069
 ProceratiinaeDiscothyrea testaceaABSCASENT0103848AMNHRAK0070
 ProceratiinaeProceratium croceumABSCASENT0104440AMNHRAK0071
 ProceratiinaeProceratium pergandeiAMNHRAK0072
 ProceratiinaeProbolomyrmex guineensisAMNHRAK0073
 PseudomyrmecinaePseudomyrmex gracilisABSCASENT0103779AMNHRAK0087
 PseudomyrmecinaeTetraponera aethiopsAMNHRAK0088
 PseudomyrmecinaeTetraponera attenuataCASCCASENT0217587AMNHRAK0089
 SphecomyrminaeSphecomyrma freyiAMNHAMNH NJ-943
SCOLIIDAEScolia nobilitataAMNHRAK0121
VESPIDAEMetapolybia cingulataAMNHRAK0120
  1. Information on museum holdings and voucher codes for queens and workers. ABS, Archbold Biological Station; ALWC, Alexander Wild Collection; AMNH, American Museum of Natural History; ANIC, Australian National Insect Collection; BMNH, British Museum of Natural History; CASC, California Academy of Science; DADC, David A. Donoso Collection; JTLC, Jack Longino Collection; MCZ, Museum of Comparative Zoology (Harvard); MIZA, Museo del Instituto de. Zoología Agrícola (Venezuela); MNHN, Muséum national d’Histoire naturelle; MSNG, Natural History Museum, Genoa; MZSP, Museu de Zoologia Universidade de São Paulo; RAJC, Robert Johnson Collection; RAKC, Roberto Keller Collection; UCDC; University of California Davis.

  2. denotes extinct taxa.

Table 3

Queen thoracic morphology and type of colony foundation across ants

SubfamilyGenusT1/T2 in queensT1 in queensColony foundingReferences
AenictinaeAenictus2.742intermediate*fission(Gotwald and Cunningham-van Someren, 1976)
AmblyoponinaeAmblyopone0.382intermediatenon-claustral(Haskins and Haskins, 1951)
AmblyoponinaeMyopopone0.453intermediatenon-claustral(Ito, 2010)
AmblyoponinaeMystrium0.454intermediatenon-claustral(Molet et al., 2009)
AmblyoponinaePrionopelta0.514intermediatenon-claustral(Ito and Billen, 1998)
AneuretinaeAneuretus0.096reducedclaustral(Wilson et al., 1956)
CerapachyinaeCerapachys0.364intermediateunknown ICF + fission(Brown, 1975)
CerapachyinaeCylindromyrmex0.454intermediatenon-claustral(Delabie and Reis, 2000)
DolichoderinaeIridomyrmex0.071reducedclaustral(Hölldobler and Carlin, 1985)
DolichoderinaeTapinoma0.111reducedclaustral(Kannowski, 1959)
DolichoderinaeTechnomyrmex0.071reducedclaustral(Yamauchi et al., 1991)
DorylinaeDorylus0.372intermediate*fission(Kronauer et al., 2004)
EcitoninaeEciton0.469intermediate*fission(Schneirla, 1949)
EctatomminaeEctatomma0.325intermediatenon-claustral(Dejean and Lachaud, 1992)
EctatomminaeRhytidoponera0.363intermediatenon-claustral(Ward, 1981)
FormicinaeFormica0.076reducedclaustral(Stille, 1996)
FormicinaeLasius0.053reducedclaustral(Stille, 1996)
FormicinaeOecophylla0.066reducedclaustral(Hölldobler and Wilson, 1978)
FormicinaePolyergus0.323intermediatenon-claustral(Mori et al., 1995)
FormicinaePolyrhachis0.072reducedclaustral and non-claustral(Lenoir and Dejean, 1994)
LeptanillinaeLeptanilla2.685intermediate*fission(Masuko, 1990)
LeptanilloidinaeLeptanilloides3.021intermediate*fission(Donoso et al., 2006)
MyrmeciinaeMyrmecia0.485intermediatenon-claustral(Haskins and Haskins, 1950)
MyrmicinaeAphaenogaster0.117reducedclaustral(Lubertazzi, 2012)
MyrmicinaeCarebara0.072reducedclaustral(Robertson and Villet, 1989)
MyrmicinaeLeptothorax0.090reducedclaustral(Keller and Passera, 1989)
MyrmicinaeMessor0.110reducedclaustral and non-claustral(Brown, 1999)
MyrmicinaeMonomorium0.132reducedclaustral(Bolton, 1986)
MyrmicinaeMyrmica0.071reducedclaustral and non-claustral(Brown and Bonhoeffer, 2003)
MyrmicinaePogonomyrmex0.097reducedclaustral and non-claustral(Johnson, 2002)
PonerinaeAnochetus0.367intermediatenon-claustral(Brown, 1978)
PonerinaeCentromyrmex0.493intermediatenon-claustral(Dejean and Fénéron, 1996)
PonerinaeCryptopone0.533intermediatenon-claustral(Peeters, 1997)
PonerinaePonera0.356intermediatenon-claustral(Kannowski, 1959)
PonerinaeMyopias0.282intermediatenon-claustral(Peeters, 1997)
PonerinaeOdontomachus0.411intermediatenon-claustral(Brown, 1976)
PonerinaeOdontoponera0.524intermediatenon-claustral(Peeters, 1997)
PonerinaePachycondyla0.385intermediatenon-claustral(Peeters, 1997)
PonerinaePlatythyrea0.417intermediatenon-claustral(Peeters, 1997)
ProceratiinaeDiscothyrea0.093reducednon-claustral and claustral(Dejean and Dejean, 1998)
  1. Queen thoracic morphology and type of colony foundation across ants. The wasp taxa Scolia and Metapolybia are included as outgroups.

  2. *

    species with wingless queens. denotes extinct taxa.

  3. Polyergus is an obligatory social parasite of Formica spp.

  4. John Lattke, personal communication.

  5. §

    Rodrigo Feitosa, personal communication.

  6. #

    Haskins CP, Enzmann EV (1937) Studies of certain sociological and physiological features in the Formicidae. Ann NY Acad Scien 37:97-162; Michael Breed, personal communication.

  7. Fuminori Ito, personal communication; Keiichi Masuko, personal communication.

  8. **

    Philip Ward, personal communication.

  9. ††

    James M Carpenter, personal communication.

Data availability

The following data sets were generated
  1. 1

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