Cryptic Lineages in the Cardiocondyla sl. kagutsuchi Terayama (Hymenoptera: Formicidae) Discovered by Phylogenetic and Morphological Approaches

Ichiro Okita, Mamoru Terayama, Koji Tsuchida

Abstract


The taxonomy of ant species in the genus Cardiocondyla is very confused due to the extreme difficulty in separating many species based on morphology alone. In Japan, one group of the species complex Cardiocondyla sl. kagutsuchi has both winged and wingless worker-like (ergatoid) males (dimorphic) whereas others have only ergatoid males (monomorphic). The presence of both groups prompted us to hypothesize that C. sl. kagutsuchi presumably includes several independent species with differences in their male wing morphologies. However, whether any species boundary actually exists between the male groups has remained unsolved over the 10+ years since the previous revision of this genus. In this study, using discriminant and phylogenetic analyses, we compared the worker caste morphology of this species complex among lineages detected by phylogenetic analyses. In addition, we examined the number of sexuals present in field colonies. Our results revealed the existence of at least three morphological and phylogenetic groups within this species complex.


Keywords


Cardiocondyla, Mitochondrial DNA, Morphology, Taxonomy

Full Text:

PDF

References


Bernasconi, C., Cherix, D., Seifert, B. & Pamilo, P. (2011). Molecular taxonomy of the Formica rufa group (red wood ants) (Hymenoptera: Formicidae): a new cryptic species in the Swiss Alps? Myrmecol. News 14: 37–47.

Besansky, N., Krzywinski, J., Lehmann, T., Simard, F., Kern, M., Mukabayire, O., Fontenille, D., Toure, Y. & N'F, S. (2003). Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. Proc. Natl. Acad. Sci. USA 100: 10818–10823. doi:10.1073/pnas.1434337100

Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22: 148–155. doi:10.1016/j.tree.2006.11.004

Bolton, B. (1982). Afrotropical species of the Myrmicinae ant genera Cardiocondyla, Leptothorax, Melissotarsus, Messor and Cataulacus (Formicidae). Bull. Br. Mus. Nat. Hist. (Ent.) 45: 307–370.

Boomsma, J.J., Baer, B.C. & Heinze, J. (2005). The evolution of male traits in social insects. Ann. Rev. Entomol. 50: 395–420. doi:10.1146/annurev.ento.50.071803.130416

Cheng, S., Kirton, L.G., Panandam, J.M., Siraj, S.S., Ng, K.K.S. & Tan, S.G. (2011). Evidence for a higher number of species of Odontotermes (Isoptera) than currently known from Peninsular Malaysia from mitochondrial DNA phylogenies. PLoS ONE 6: e20992. doi:10.1371/journal.pone.0020992

Cheung, W., Hubert, N. & Landry, B. (1993). A simple and rapid DNA microextraction method for plant, animal, and insect suitable for RAPD and other PCR analyses. Genome Res. 3: 69–70.

Cremer, S., Sledge, M. & Heinze, J. (2002). Chemical mimicry: Male ants disguised by the queens’ bouquet. Nature 419: 897. doi:10.1038/419897a

Frohchammer, S. & Heinze, J. (2009). A heritable component in sex ratio and caste determination in a Cardiocondyla ant. Front. Zool. 6: 27. doi:10.1186/1742-9994-6-27

Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the Neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. USA 101: 14812–14817. doi:10.1073/pnas.0406166101

Heinze, J., Holldobler, B. & Yamauchi, K. (1998). Male competition in Cardiocondyla ants. Behav. Ecol. Sociobiol. 42: 239–246.

Heinze, J., Trindl, A., Seifert, B. & Yamauchi, K. (2005). Evolution of male morphology in the ant genus Cardiocondyla. Mol. Phylogenet. Evol. 37: 278–288. doi:10.1016/j.ympev.2005.04.005

Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120.

Kinomura, K. & Yamauchi, K. (1987). Fighting and mating behaviors of dimorphic males in the ant. J. Ethol. 5: 75–81.

Kugler, J. (1983). The males of Cardiocondyla Emery (Hymenoptera: Formicidae) with the description of the winged male of Cardiocondyla wroughtonii (Forel). Isr. J. Entomol. 17: 1–21.

Lenoir, J.C., Schrempf, A., Lenoir, A., , J. & Mercier, J.L. (2007). Genetic structure and reproductive strategy of the ant Cardiocondyla elegans: strictly monogynous nests invaded by unrelated sexuals. Mol. Ecol. 16: 345–354. doi:10.1111/j.1365-294X.2006.03156.x

Molbo, D., Machado, C.A., Sevenster, J.G., Keller, L. & Herre, E.A. (2003). Cryptic species of fig-pollinating wasps: implications for the evolution of the fig–wasp mutualism, sex allocation, and precision of adaptation. Proc. Natl. Acad. Sci. USA 100: 5867–5872. doi:10.1073/pnas.0930903100

Murray, T.E., Fitzpatrick, U., Brown, M.J.F. & Paxton, R.J. (2008). Cryptic species diversity in a widespread bumble bee complex revealed using mitochondrial DNA RFLPs. Cons. Genet. 9: 653–666. doi:10.1007/s10592-007-9394-z

Nylander, J.A.A. (2004). MrModeltest ver. 2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. (Available from: https://github.com/nylander/MrModeltest2)

Oettler, J., Suefuji, M., & Heinze, J. (2010). The evolution of alternative reproductive tactics in male Cardiocondyla ants. Evolution 64: 3310-3317. doi:10.1111/j.1558-5646.2010.01090.x

Okita, I., Murase, K., Sato, T., Kato, K., Hosoda, A., Terayama, M., & Masuko, K. (2013). The spatial distribution of mtDNA and phylogeographic analysis of the ant Cardiocondyla kagutsuchi (Hymenoptera: Formicidae) in Japan. Sociobiology 60: 129–134. doi:10.13102/sociobiology.v60i2.129-134

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542. doi:10.1093/sysbio/sys029

Ross, K.G., Gotzek, D., Ascunce, M.S. & Shoemaker, D.D.W. 2010. Species delimitation: a case study in a problematic ant taxon. Syst. Biol. 59: 162–184. doi:10.1093/sysbio/syp089

Schlick-Steiner, B.C., Steiner, F.M., Moder, K., Seifert, B., Sanetra, M., Dyreson, E., Stauffer, C. & Christian, E. (2006). A multidisciplinary approach reveals cryptic diversity in Western Palearctic Tetramorium ants (Hymenoptera: Formicidae). Mol. Phylogenet. Evol. 40: 259–273.

doi:10.1016/j.ympev.2006.03.005

Schrempf, A., Reber, C., Tinaut, A. & Heinze, J. (2005). Inbreeding and local mate competition in the ant Cardiocondyla batesii. Behav. Ecol. Sociobiol. 57: 502–510. doi:10.1007/s00265-004-0869-3

Seifert, B. (2003). The ant genus Cardiocondyla (Insecta: Hymenoptera: Formicidae)—a taxonomic revision of the C. elegans, C. bulgarica, C. batesii, C. nuda, C. shuckardi, C. stambuloffii, C. wroughtonii, C. emeryi and C. minutior species groups. Ann. Naturhist. Mus. Wien 104(B): 203–338.

Seifert, B. (2008). Cardiocondyla atalanta FOREL, 1915, a cryptic sister species of Cardiocondyla nuda (MAYR, 1866) (Hymenoptera: Formicidae). Myrmecol. News 11: 43–48.

Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87: 651–701.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731–2739. doi:10.1093/molbev/msr121

Terayama, M. (1999). Taxonomic studies of the Japanese Formicidae, part 6. Genus Cardiocondyla Emery. Mem. Myrmecol. Soc. Jpn. 1: 99–107.

Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680.

Yamane, Sk. (2010). Collecting, preparing and identifying ant specimens. In Yamane, Sk., Harada, Y., Eguchi, K. (Eds.), Natural History of Ants in South Kyushu (pp. 170–171). Japan, Nanpo-sinsha, Kagoshima. (In Japanese)

Yamauchi, K. & Kawase, N. (1992). Pheromonal manipulation of workers by a fighting male to kill his rival males in the ant Cardiocondyla wroughtonii. Naturwissenschaften 79: 274–276.

Yamauchi, K. & Kinomura, K. (1993). Lethal fighting and reproductive strategy of dimorphic males in Cardiocondyla ants (Hymenoptera: Formicidae). In Inoue, T., Yamane, Sk. (Eds.), Evolution of Insect Societies (pp. 373–402). Hakuhinsya, Tokyo. (In Japanese)

Yamauchi, K., Asano, Y., Lautenschlager, B., Trindl, A. & Heinze, J. (2005). A new type of male dimorphism with ergatoid and short-winged males in Cardiocondyla cf. kagutsuchi. Insect. Soc. 52: 274–281. doi:10.1007/s00040-005-0803-3

Yamauchi, K., Ishida, Y., Hashim, R. & Heinze, J. (2007). Queen–queen competition and reproductive skew in a Cardiocondyla ant. Insect. Soc. 54: 268–274. doi:10.1007/s00040-007-0941-x

Yashiro, T., Matsuura, K., Guenard, B., Terayama, M. & Dunn, R.R. (2010). On the evolution of the species complex Pachycondyla chinensis (Hymenoptera: Formicidae: Ponerinae), including the origin of its invasive form and description of a new species. Zootaxa 2685: 39–50.




DOI: http://dx.doi.org/10.13102/sociobiology.v62i3.805

Refbacks

  • There are currently no refbacks.


JCR Impact Factor 2018: 0.604