Where Fossils Dare and Males Matter: combined morphological and molecular analysis untangles the evolutionary history of the spider ant genus Leptomyrmex Mayr (Hymenoptera : Dolichoderinae)
Phillip Barden A B E , Brendon Boudinot C and Andrea Lucky D
+ Author Affiliations
- Author Affiliations
A Department of Biological Sciences, Rutgers University, Newark, NJ 07102, USA.
B Richard Gilder Graduate School, American Museum of Natural History, New York, NY 10024, USA.
C Department of Entomology and Center for Population Biology, University of California, Davis, CA 95616, USA.
D Entomology and Nematology Department, University of Florida, Gainesville, FL 32611, USA.
E Corresponding author. Present address: Department of Biological Sciences, New Jersey Institute of Technology, Newark, NJ, USA. Email: pbarden@amnh.org
Invertebrate Systematics 31(6) 765-780 https://doi.org/10.1071/IS16067
Submitted: 22 September 2016 Accepted: 9 April 2017 Published: 29 November 2017
Abstract
The distinctive ant genus Leptomyrmex Mayr, 1862 had been thought to be endemic to Australasia for over 150 years, but enigmatic Neotropical fossils have challenged this view for decades. The present study responds to a recent and surprising discovery of extant Leptomyrmex species in Brazil with a thorough evaluation of the Dominican Republic fossil material, which dates to the Miocene. In the first case study of direct fossil inclusion within Formicidae Latreille, 1809, we incorporated both living and the extinct Leptomyrmex species. Through simultaneous analysis of molecular and morphological characters in both Bayesian and parsimony frameworks, we recovered the fossil taxon as sister-group to extant Leptomyrmex in Brazil while considering the influence of taxonomic and character sampling on inferred hypotheses relating to tree topology, biogeography and morphological evolution. We also identified potential loss of signal in the binning of morphological characters and tested the impact of parameterisation on divergence date estimation. Our results highlight the importance of securing sufficient taxon sampling for extant lineages when incorporating fossils and underscore the utility of diverse character sources in accurate placement of fossil terminals. Specifically, we find that fossil placement in this group is influenced by the inclusion of male-based characters and the newly discovered Neotropical ‘Lazarus taxon’.
Additional keywords: biogeography, character discretisation, genitalia, male morphology, paleontology, tip-dating, total evidence.
References
Arcila, D., Pyron, R. A., Tyler, J. C., Ortí, G., and Betancur-R, R. (2015). An evaluation of fossil tip-dating versus node-age calibrations in tetraodontiform fishes (Teleostei: Percomorphaceae). Molecular Phylogenetics and Evolution 82, 131–145.| An evaluation of fossil tip-dating versus node-age calibrations in tetraodontiform fishes (Teleostei: Percomorphaceae).Crossref | GoogleScholarGoogle Scholar |
Baroni Urbani, C. (1980). The first fossil species of the Australian ant genus Leptomyrmex in amber from the Dominican Republic. Stuttgarter Beiträge zur Naturkunde, Serie B 62, 1–10.
Baroni Urbani, C., and Wilson, E. O. (1987). The fossil members of the ant tribe Leptomyrmicini (Hymenoptera: Formicidae). Psyche 94, 1–8.
| The fossil members of the ant tribe Leptomyrmicini (Hymenoptera: Formicidae).Crossref | GoogleScholarGoogle Scholar |
Boudinot, B. E (2013). The male genitalia of ants: musculature, homology, and functional morphology (Hymenoptera, Aculeata, Formicidae). Journal of Hymenoptera Research 30, 29–49.
| The male genitalia of ants: musculature, homology, and functional morphology (Hymenoptera, Aculeata, Formicidae).Crossref | GoogleScholarGoogle Scholar |
Boudinot, B. E. (2015). Contributions to the knowledge of Formicidae (Hymenoptera, Aculeata): a new diagnosis of the family, the first global male-based key to subfamilies, and a treatment of early branching lineages. European Journal of Taxonomy 120, 1–62.
Boudinot, B. E., Probst, R. S., Brandão, C. R. F., Feitosa, R. M., and Ward, P. S. (2016). Out of the Neotropics: newly discovered relictual species sheds light on the biogeographic history of spider ants (Leptomyrmex, Dolichoderinae, Formicidae). Systematic Entomology 41, 658–671.
| Out of the Neotropics: newly discovered relictual species sheds light on the biogeographic history of spider ants (Leptomyrmex, Dolichoderinae, Formicidae).Crossref | GoogleScholarGoogle Scholar |
Brady, S. G. (2011). Effects of fossil calibration uncertainty on divergence dating of ants and bees. American Entomologist 57, 56–57.
| Effects of fossil calibration uncertainty on divergence dating of ants and bees.Crossref | GoogleScholarGoogle Scholar |
Brody, R. H., Edwards, H. G., and Pollard, A. M. (2001). A study of amber and copal samples using FT-Raman spectroscopy. Spectrochimica Acta. Part A: Molecular and Biomolecular Spectroscopy 57, 1325–1338.
| A study of amber and copal samples using FT-Raman spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2FhsVOnug%3D%3D&md5=49936a405f89c7d2dc20fb679b796231CAS |
Brown, WL, Jr., and Nutting, WL (1950). Wing venation and the phylogeny of the Formicidae. Transactions of the American Entomological Society 75, 113–132.
Dawson, M. R., Marivaux, L., Li, C. K., Beard, K. C., and Métais, G. (2006). Laonastes and the “Lazarus effect” in recent mammals. Science 311, 1456–1458.
| Laonastes and the “Lazarus effect” in recent mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVyjsLs%3D&md5=2576d1404c76750f61364c3b5ea8caa4CAS |
DeConto, R. M., and Pollard, D. (2003). Rapid Cenozoic glaciation of Antarctica induced by declining atmospheric CO2. Nature 421, 245–249.
| Rapid Cenozoic glaciation of Antarctica induced by declining atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsF2hug%3D%3D&md5=7c1c5888e151524225eac4f0e11fcbedCAS |
Dlussky, G., Radchenko, A., and Dubovikoff, D. (2014). A new enigmatic ant genus from late Eocene Danish amber and its evolutionary and zoogeographic significance. Acta Palaeontologica Polonica 59, 931–939.
Donoghue, P. C., and Benton, M. J. (2007). Rocks and clocks: calibrating the Tree of Life using fossils and molecules. Trends in Ecology & Evolution 22, 424–431.
| Rocks and clocks: calibrating the Tree of Life using fossils and molecules.Crossref | GoogleScholarGoogle Scholar |
Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar |
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=3779829e13a4c162ef008e41e63c789fCAS |
Eernisse, D. J., and Kluge, A. G. (1993). Taxonomic congruence versus total evidence, and amniote phylogeny inferred from fossils, molecules, and morphology. Molecular Biology and Evolution 10, 1170–1195.
| 1:CAS:528:DyaK2cXisF2gsw%3D%3D&md5=5999906a99d3762d08d7af2f0af2c6dfCAS |
Emerson, A. E. (1965). A review of the Mastotermitidae (Isoptera), including a new fossil genus from Brazil. American Museum Novitates 2236, 1–46.
Emery, C. (1891). Le formiche dell’ambra Siciliana nel Museo Mineralogico dell’Universita di Bologna. Accademia delle Scienze dell’Istituto di Bologna 5, 141–165.
Emery, C. (1913). Hymenoptera family Formicidae subfamily Dolichoderinae. Genera Insectorum 137, 1–50.
Goloboff, P. A., Farris, J. S., Källersjö, M., Oxelman, B., and Szumik, C. A. (2003). Improvements to resampling measures of group support. Cladistics 19, 324–332.
| Improvements to resampling measures of group support.Crossref | GoogleScholarGoogle Scholar |
Goloboff, P. A., Farris, J. S., and Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786.
| TNT, a free program for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |
Grimaldi, D., and Engel, M. S. (2005). ‘Evolution of the Insects.’ (Cambridge University Press: New York.)
Grimaldi, D., Engel, M. S., Nascimbene, P. C., and Singh, H. (2013). Coniopterygidae (Neuroptera: Aleuropteryginae) in amber from the Eocene of India and the Miocene of Hispaniola. American Museum Novitates 3770, 20–39.
| Coniopterygidae (Neuroptera: Aleuropteryginae) in amber from the Eocene of India and the Miocene of Hispaniola.Crossref | GoogleScholarGoogle Scholar |
Grossi, P. C., and Aguiar, N. O. (2014). Discovery of a third stag beetle genus in the Amazonian region, with description of a new species of Psilodon Perty (Coleoptera: Lucanidae: Syndesinae: Syndesini). Coleopterists Bulletin 68, 83–90.
| Discovery of a third stag beetle genus in the Amazonian region, with description of a new species of Psilodon Perty (Coleoptera: Lucanidae: Syndesinae: Syndesini).Crossref | GoogleScholarGoogle Scholar |
Katz, M. E., Miller, K. G., Wright, J. D., Wade, B. S., Browning, J. V., Cramer, B. S., and Rosenthal, Y. (2008). Stepwise transition from the Eocene greenhouse to the Oligocene icehouse. Nature Geoscience 1, 329–334.
| Stepwise transition from the Eocene greenhouse to the Oligocene icehouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltlCksLg%3D&md5=f6f36e2d2fc69412f2a0b81cd6b472dbCAS |
Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
| PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=60257dbe2868778a4d0b3f3c019d85e1CAS |
Lepage, T., Bryant, D., Philippe, H., and Lartillot, N. (2007). A general comparison of relaxed molecular clock models. Molecular Biology and Evolution 24, 2669–2680.
| A general comparison of relaxed molecular clock models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVGisg%3D%3D&md5=df8a1324137ed6f0a437b0b2b38f45f3CAS |
Lewis, P. O. (2001). A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50, 913–925.
| A likelihood approach to estimating phylogeny from discrete morphological character data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntVKlsQ%3D%3D&md5=4119815f54bbe0f2fee6ccde3b44bbdaCAS |
Lucky, A. (2011). Molecular phylogeny and biogeography of the spider ants, genus Leptomyrmex Mayr (Hymenoptera: Formicidae). Molecular Phylogenetics and Evolution 59, 281–292.
| Molecular phylogeny and biogeography of the spider ants, genus Leptomyrmex Mayr (Hymenoptera: Formicidae).Crossref | GoogleScholarGoogle Scholar |
Lucky, A., and Ward, P. S. (2010). Taxonomic revision of the ant genus Leptomyrmex Mayr (Hymenoptera: Formicidae). Zootaxa 2688, 1–67.
McKellar, R. C., Glasier, J. R., and Engel, M. S. (2013). New ants (Hymenoptera: Formicidae: Dolichoderinae) from Canadian Late Cretaceous amber. Bulletin of Geosciences 88, 583–594.
| New ants (Hymenoptera: Formicidae: Dolichoderinae) from Canadian Late Cretaceous amber.Crossref | GoogleScholarGoogle Scholar |
Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE)’, 14 November 2010, New Orleans, LA. pp. 1–8. (Institute of Electrical and Electronics Engineers: Piscataway, NJ.) Available at http://ieeexplore.ieee.org/document/5676129/?tp=&arnumber=5676129&filter%3DAND(p_IS_Number:5676117) [Verified July 2017]
Petrulevičius, J. F., and Nel, A. (2009). First Cordulephyidae dragonfly in America: a new genus and species from the Paleogene of Argentina (Insecta: Odonata). Comptes Rendus. Palévol 8, 385–388.
| First Cordulephyidae dragonfly in America: a new genus and species from the Paleogene of Argentina (Insecta: Odonata).Crossref | GoogleScholarGoogle Scholar |
Pyron, R. A. (2011). Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Systematic Biology 60, 466–481.
| Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A. (2014) FigTree. Available at http://tree.bio.ed.ac.uk [Verified July 2017].
Rambaut, A., and Drummond, A. J. (2010) TreeAnnotator. Available at http://beast.bio.ed.ac.uk [Verified July 2017].
Rambaut, A., Suchard, M., and Drummond, A. J. (2013) Tracer. Available at http:/tree.bio.ed.ac.uk [Verified July 2017].
Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=551961d8686b21e6a8f449a4435c2cfdCAS |
Ronquist, F., Klopfstein, S., Vilhelmsen, L., Schulmeister, S., Murray, D. L., and Rasnitsyn, A. P. (2012). A total-evidence approach to dating with fossils, applied to the early radiation of the Hymenoptera. Systematic Biology 61, 973–999.
Royer, D. L., Hickey, L. J., and Wing, S. L. (2003). Ecological conservatism in the “living fossil” Ginkgo. Paleobiology 29, 84–104.
| Ecological conservatism in the “living fossil” Ginkgo.Crossref | GoogleScholarGoogle Scholar |
Rutschmann, F., Eriksson, T., Salim, K. A., and Conti, E. (2007). Assessing calibration uncertainty in molecular dating: the assignment of fossils to alternative calibration points. Systematic Biology 56, 591–608.
| Assessing calibration uncertainty in molecular dating: the assignment of fossils to alternative calibration points.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKrs7%2FK&md5=850198b31dab5b4721fb9932ba621f77CAS |
Sanmartín, I., and Ronquist, F. (2004). Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology 53, 216–243.
| Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns.Crossref | GoogleScholarGoogle Scholar |
Shattuck, S. O. (1992). Generic revision of the ant subfamily Dolichoderinae (Hymenoptera: Formicidae). Sociobiology 21, 1–181.
Shattuck, S. (2000). ‘Australian Ants: their Biology and Identification. Vol. 3.’ (CSIRO Publishing: Melbourne.)
Smith, D. J., and Shattuck, S. (2009). Six new, unusually small ants of the genus Leptomyrmex (Hymenoptera: Formicidae). Zootaxa 2142, 57–68.
Sturm, H., and Mendes, L. F. (1998). Two new species of Nicoletiidae (Zygentoma, “Apterygota,” Insecta) in Dominican amber. American Museum Novitates 3226, 1–11.
Ward, P. S., Brady, S. G., Fisher, B. L., and Schultz, T. R. (2010). Phylogeny and biogeography of dolichoderine ants: effects of data partitioning and relict taxa on historical inference. Systematic Biology 59, 342–362.
| Phylogeny and biogeography of dolichoderine ants: effects of data partitioning and relict taxa on historical inference.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Kms7o%3D&md5=9ffdca389c39b1541d1a7eb6445dbf87CAS |
Ward, P. S., Blaimer, B. B., and Fisher, B. L. (2016). A revised phylogenetic classification of the ant subfamily Formicinae (Hymenoptera: Formicidae), with resurrection of the genera Colobopsis and Dinomyrmex. Zootaxa 4072, 343–357.
| A revised phylogenetic classification of the ant subfamily Formicinae (Hymenoptera: Formicidae), with resurrection of the genera Colobopsis and Dinomyrmex.Crossref | GoogleScholarGoogle Scholar |
Ware, J. L., Grimaldi, D. A., and Engel, M. S. (2010). The effects of fossil placement and calibration on divergence times and rates: an example from the termites (Insecta: Isoptera). Arthropod Structure & Development 39, 204–219.
| The effects of fossil placement and calibration on divergence times and rates: an example from the termites (Insecta: Isoptera).Crossref | GoogleScholarGoogle Scholar |
Wheeler, W. M. (1915). The Australian honey-ants of the genus Leptomyrmex Mayr. Proceedings of the American Academy of Arts and Sciences 51, 255–286.
| The Australian honey-ants of the genus Leptomyrmex Mayr.Crossref | GoogleScholarGoogle Scholar |
Wheeler, W. M. (1934). A second revision of the ants of the genus Leptomyrmex Mayr. Bulletin of the Museum of Comparative Zoology 77, 69–118.
Wiens, J. J. (2003). Missing data, incomplete taxa, and phylogenetic accuracy. Systematic Biology 52, 528–538.
| Missing data, incomplete taxa, and phylogenetic accuracy.Crossref | GoogleScholarGoogle Scholar |
Wiens, J. J. (2006). Missing data and the design of phylogenetic analyses. Journal of Biomedical Informatics 39, 34–42.
| Missing data and the design of phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotVGgsQ%3D%3D&md5=6238fa502b44bbb5f87f27554a0ec77dCAS |
Wiens, J. J., and Morrill, M. C. (2011). Missing data in phylogenetic analysis: reconciling results from simulations and empirical data. Systematic Biology 60, 719–731.
| Missing data in phylogenetic analysis: reconciling results from simulations and empirical data.Crossref | GoogleScholarGoogle Scholar |
Wilson, E. O. (1985). Ants of the Dominican amber (Hymenoptera: Formicidae). 3. The subfamily Dolichoderinae. Psyche 92, 17–37.
| Ants of the Dominican amber (Hymenoptera: Formicidae). 3. The subfamily Dolichoderinae.Crossref | GoogleScholarGoogle Scholar |
Wood, H. M., Matzke, N. J., Gillespie, R. G., and Griswold, C. E. (2013). Treating fossils as terminal taxa in divergence time estimation reveals ancient vicariance patterns in the palpimanoid spiders. Systematic Biology 62, 264–284.
| Treating fossils as terminal taxa in divergence time estimation reveals ancient vicariance patterns in the palpimanoid spiders.Crossref | GoogleScholarGoogle Scholar |
Woodruff, R. E. (2009). A new fossil species of stag beetle from Dominican Republic amber, with Australasian connections (Coleoptera: Lucanidae). Insecta Mundi 98, 1–10.
Zheng, Y., and Wiens, J. J. (2015). Do missing data influence the accuracy of divergence-time estimation with BEAST? Molecular Phylogenetics and Evolution 85, 41–49.
| Do missing data influence the accuracy of divergence-time estimation with BEAST?Crossref | GoogleScholarGoogle Scholar |
