Cryptic Lineages in the Cardiocondyla sl. kagutsuchi Terayama (Hymenoptera: Formicidae) Discovered by Phylogenetic and Morphological Approaches
DOI:
https://doi.org/10.13102/sociobiology.v62i3.805Keywords:
Cardiocondyla, Mitochondrial DNA, Morphology, TaxonomyAbstract
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.
Downloads
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.
Downloads
Published
How to Cite
Issue
Section
License
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).