Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

eadem figura manet: Measuring morphological convergence in diplocentrid scorpions (Arachnida : Scorpiones : Diplocentridae) under a multilocus phylogenetic framework

Carlos E. Santibáñez-López A C D , Ricardo Kriebel B C and Prashant P. Sharma A
+ Author Affiliations
- Author Affiliations

A Department of Zoology, University of Wisconsin – Madison, 430 Lincoln Drive, Madison, WI 53706, USA.

B Department of Botany, University of Wisconsin – Madison, 430 Lincoln Drive, Madison, WI 53706, USA.

C Authors contributed equally to this work.

D Corresponding author. Email: santibanezlo@wisc.edu

Invertebrate Systematics 31(3) 233-248 https://doi.org/10.1071/IS16078
Submitted: 19 November 2016  Accepted: 15 January 2017   Published: 2 May 2017

Abstract

Morphology still plays a key role in the systematics and phylogenetics of most of the scorpion families and genera, including the Diplocentridae Karsch, 1880. The monophyly of this family, and the monophyly of its two subfamilies is supported by morphological characters; however, neither hypothesis has been tested using molecular data. The lack of a molecular phylogeny has prevented the study of the evolution of morphology within the family. Here, we examine the morphological evolution of several key character systems in diplocentrid systematics. We tested the monophyly of the Diplocentridae, and subsequently the validity of its two subfamilies using a five-locus phylogeny. We examined the variation and evolution of the shape of the carapace, the external surface of the pedipalp patella and the retrolateral surface of the pedipalp chelae of males and females. We also examined the phylogenetic signal of discrete and continuous characters previously reported. We show that Diplocentridae is monophyletic, but Nebinae is nested within Diplocentrinae. Therefore, Nebinae is synonymised with Diplocentrinae (new synonymy). Finally, we show that a new character system proposed here, tarsal spiniform and macrosetal counts, retains high phylogenetic signal and circumscribes independently evolving substructures within this character system.

Additional keywords: comparative methods, dated phylogeny, phylogenetic signal, trait correlation.


References

Abouheif, E. (1999). A method for testing the assumption of phylogenetic independence in comparative data. Evolutionary Ecology Research 1, 895–909. open url image1

Agolin, M., and D’Haese, C. A. (2009). An application of dynamic homology to morphological characters: direct optimization of setae sequences and phylogeny of the family Odontellidae (Poduromorpha, Collembola). Cladistics 25, 353–385.
An application of dynamic homology to morphological characters: direct optimization of setae sequences and phylogeny of the family Odontellidae (Poduromorpha, Collembola).CrossRef | open url image1

Blomberg, S. P., Garland, T., and Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745.
Testing for phylogenetic signal in comparative data: behavioral traits are more labile.CrossRef | open url image1

Bonhomme, V., Picq, S., Gaucherel, C., and Claude, J. (2014). Momocs: outline analysis using R. Journal of Statistical Software 56, 1–24.
Momocs: outline analysis using R.CrossRef | open url image1

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.CrossRef | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=12c15c65b143ca193ea00e1aa007f6b7CAS | open url image1

Chessel, D., Dufour, A. B., and Thioulouse, J. (2004). The ade4 package-I- one-table methods. R News 4, 5–10. open url image1

Coddington, J. A., Giribet, G., Harvey, M. S., Prendini, L., and Walter, D. E. (2004). Arachnida. In ‘Assembling the Tree of Life’. (Eds J. Cracraft and P. C. J. Donoghue.) pp. 296–318. (Oxford University Press: New York.)

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.CrossRef | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=1e151a811e335310e17f8244e6b6ccbaCAS | open url image1

Drummond, A. J., Ho, S., Phillips, M. J., and Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.
Relaxed phylogenetics and dating with confidence.CrossRef | open url image1

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.CrossRef | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=1128fe2c54a768f2b18bd3a1ecbe3c88CAS | open url image1

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 | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=3779829e13a4c162ef008e41e63c789fCAS | open url image1

Fet, V., Gantenbein, B., Gromov, A., Lowe, G., and Lourenço, W. R. (2003). The first molecular phylogeny of Buthidae (Scorpiones). Euscorpius 4, 1–10. open url image1

Francke, O. F. (1977a). Taxonomic observations on Heteronebo Pocock (Scorpionida, Diplocentridae). The Journal of Arachnology 4, 95–113. open url image1

Francke, O. F. (1977b). Scorpions of the genus Diplocentrus from Oaxaca, Mexico (Scorpionida, Diplocentridae). The Journal of Arachnology 4, 145–200. open url image1

Francke, O. F. (1978). Systematic revision of diplocentrid scorpions (Diplocentridae) from circum-Caribbean lands. Special Publications The Museum Texas Tech University 14, 1–92. open url image1

Francke, O. F. (1980). Revision of the genus Nebo Simon (Scorpiones: Diplocentridae). The Journal of Arachnology 8, 35–52. open url image1

Francke, O. F., and Prendini, L. (2008). Phylogeny and classification of the giant hairy scorpions, Hadrurus Thorell (Iuridae Thorell): a reappraisal. Systematics and Biodiversity 6, 205–223.
Phylogeny and classification of the giant hairy scorpions, Hadrurus Thorell (Iuridae Thorell): a reappraisal.CrossRef | open url image1

Francke, O. F., Teruel, R., and Santibáñez-López, C. E. (2014). A new genus and a new species of scorpion (Scorpiones: Buthidae) from southeastern Mexico. The Journal of Arachnology 42, 220–232.
A new genus and a new species of scorpion (Scorpiones: Buthidae) from southeastern Mexico.CrossRef | open url image1

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 | open url image1

González-Santillán, E., and Prendini, L. (2015). Phylogeny of the North American vaejovid scorpion subfamily Syntropinae Kraepelin, 1905, based on morphology, mitochondrial and nuclear DNA. Cladistics 31, 341–405.
Phylogeny of the North American vaejovid scorpion subfamily Syntropinae Kraepelin, 1905, based on morphology, mitochondrial and nuclear DNA.CrossRef | open url image1

Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.CrossRef | open url image1

Hendrixson, B. E. (2006). Buthid scorpions of Saudi Arabia, with notes on other families (Scorpiones: Buthidae, Liochelidae, Scorpionidae). Fauna of Saudi Arabia 21, 33–120. open url image1

Keck, F., Rimet, F., Bouchez, A., and Franc, A. (2016). phylosignal: an R package to measure, test, and explore the phylogenetic signal. Ecology and Evolution 6, 2774–2780.
phylosignal: an R package to measure, test, and explore the phylogenetic signal.CrossRef | open url image1

Maddison, W. P., and Maddison, D. R. (2016). Mesquite: a modular system for evolutionary analysis. Version 3.10. Available at http://mesquiteproject.org.

Mattoni, C., Ochoa, J., Ojanguren-Affilastro, A., and Prendini, L. (2010). Towards an all-species phylogeny of the scorpion family Bothriuridae. Cladistics 26, 216–217. open url image1

Monod, L., and Prendini, L. (2015). Evidence for Eurogondwana: the roles of dispersal, extinction and vicariance in the evolution and biogeography of Indo-Pacific Hormuridae (Scorpiones: Scorpionoidea). Cladistics 31, 71–111.
Evidence for Eurogondwana: the roles of dispersal, extinction and vicariance in the evolution and biogeography of Indo-Pacific Hormuridae (Scorpiones: Scorpionoidea).CrossRef | open url image1

Münkemüller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K., and Thuiller, W. (2012). How to measure and test phylogenetic signal. Methods in Ecology and Evolution 3, 743–756.
How to measure and test phylogenetic signal.CrossRef | open url image1

Ojanguren-Affilastro, A. A., Mattoni, C. I., Ochoa, J. A., Ramírez, M. J., Ceccarelli, F. S., and Prendini, L. (2016). Phylogeny, species delimitation and convergence in the South American bothriurid scorpion genus Brachistosternus Pocock 1893: integrating morphology, nuclear and mitochondrial DNA. Molecular Phylogenetics and Evolution 94, 159–170.
Phylogeny, species delimitation and convergence in the South American bothriurid scorpion genus Brachistosternus Pocock 1893: integrating morphology, nuclear and mitochondrial DNA.CrossRef | open url image1

Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature 401, 877–884.
Inferring the historical patterns of biological evolution.CrossRef | 1:CAS:528:DyaK1MXntFymtL8%3D&md5=b5b652287d2718033ba064b4119c53d5CAS | open url image1

Pagel, M., and Meade, A. (2006). Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov Chain Monte Carlo. American Naturalist 167, 808–825. open url image1

Pavoine, S., Ollier, S., Pontier, D., and Chessel, D. (2008). Testing for phylogenetic signal in phenotypic traits: new matrices of phylogenetic proximities. Theoretical Population Biology 73, 79–91.
Testing for phylogenetic signal in phenotypic traits: new matrices of phylogenetic proximities.CrossRef | open url image1

Posada, D., and Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793–808.
Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests.CrossRef | open url image1

Prendini, L. (2000). Phylogeny and classification of the superfamily Scorpionoidea Latreille 1802 (Chelicerata, Scorpiones): an exemplar approach. Cladistics 16, 1–78.
Phylogeny and classification of the superfamily Scorpionoidea Latreille 1802 (Chelicerata, Scorpiones): an exemplar approach.CrossRef | open url image1

Prendini, L. (2003). A new genus and species of bothriurid scorpion from the Brandberg Massif, Namibia, with a reanalysis of bothriurid phylogeny and a discussion of the phylogenetic position of Lisposoma Lawrence. Systematic Entomology 28, 149–172.
A new genus and species of bothriurid scorpion from the Brandberg Massif, Namibia, with a reanalysis of bothriurid phylogeny and a discussion of the phylogenetic position of Lisposoma Lawrence.CrossRef | open url image1

Prendini, L., and Esposito, L. A. (2010). A reanalysis of Parabuthus (Scorpiones: Buthidae) phylogeny with descriptions of two new Parabuthus species endemic to the Central Namib gravel plains, Namibia. Zoological Journal of the Linnean Society 159, 673–710. open url image1

Prendini, L., and Wheeler, W. C. (2004). Assembling the scorpion tree of life: phylogeny of extant scorpions based on molecules, morphology and exemplars. Cladistics 20, 602–603. open url image1

Prendini, L., Crowe, T. M., and Wheeler, W. C. (2003). Systematics and biogeography of the family Scorpionidae (Chelicerata: Scorpiones), with a discussion on phylogenetic methods. Invertebrate Systematics 17, 185–259.
Systematics and biogeography of the family Scorpionidae (Chelicerata: Scorpiones), with a discussion on phylogenetic methods.CrossRef | 1:CAS:528:DC%2BD3sXmslals7o%3D&md5=71fa9d340447aede75696c7348673cddCAS | open url image1

Prendini, L., Francke, O. F., and Vignoli, V. (2010). Troglomorphism, trichobothriotaxy and typhlochactid phylogeny (Scorpiones, Chactoidea): more evidence that troglobitism is not an evolutionary dead-end. Cladistics 26, 117–142.
Troglomorphism, trichobothriotaxy and typhlochactid phylogeny (Scorpiones, Chactoidea): more evidence that troglobitism is not an evolutionary dead-end.CrossRef | open url image1

Rambaut, A., Suchard, M. A., Xie, D., and Drummond, A. J. (2014). Tracer v1.6. Available at http://beast.bio.ed.ac.uk/Tracer.

Revell, L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217–223.
phytools: an R package for phylogenetic comparative biology (and other things).CrossRef | open url image1

Robinson, D. F., and Foulds, L. R. (1981). Comparison of phylogenetic trees. Mathematical Biosciences 53, 131–147.
Comparison of phylogenetic trees.CrossRef | open url image1

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.CrossRef | open url image1

Santibáñez-López, C. E. (2014). A new species of the genus Diplocentrus Peters, 1861 (Scorpiones, Diplocentridae) from Oaxaca, Mexico. ZooKeys 412, 103–116.
A new species of the genus Diplocentrus Peters, 1861 (Scorpiones, Diplocentridae) from Oaxaca, Mexico.CrossRef | open url image1

Santibáñez-López, C. E., and Francke, O. F. (2013). Redescription of Diplocentrus zacatecanus (Scorpiones: Diplocentridae) and limitations of the hemispermatophore as a diagnostic trait for genus Diplocentrus. The Journal of Arachnology 41, 1–10.
Redescription of Diplocentrus zacatecanus (Scorpiones: Diplocentridae) and limitations of the hemispermatophore as a diagnostic trait for genus Diplocentrus.CrossRef | open url image1

Santibáñez-López, C. E., Francke, O. F., and Prendini, L. (2013a). Systematics of the keyserlingii group of Diplocentrus Peters, 1861 (Scorpiones: Diplocentridae), with descriptions of three new species from Oaxaca, Mexico. American Museum Novitates 3777, 1–48.
Systematics of the keyserlingii group of Diplocentrus Peters, 1861 (Scorpiones: Diplocentridae), with descriptions of three new species from Oaxaca, Mexico.CrossRef | open url image1

Santibáñez-López, C. E., Francke, O. F. B., and Ortega-Gutierrez, A. (2013b). Variation in the spiniform macrosetae pattern on the basitarsi of Diplocentrus tehuacanus (Scorpiones: Diplocentridae): new characters to diagnose species within the genus. The Journal of Arachnology 41, 319–326.
Variation in the spiniform macrosetae pattern on the basitarsi of Diplocentrus tehuacanus (Scorpiones: Diplocentridae): new characters to diagnose species within the genus.CrossRef | open url image1

Santibáñez-López, C. E., Francke, O. F., and Prendini, L. (2014a). Phylogeny of the North American scorpion genus Diplocentrus Peters, 1861 (Scorpiones: Diplocentridae) based on morphology, nuclear and mitochondrial DNA. Arthropod Systematics & Phylogeny 72, 257–279. open url image1

Santibáñez-López, C. E., Francke, O. F., and Prendini, L. (2014b). Kolotl, n. gen. (Scorpiones: Diplocentridae), a new scorpion genus from Mexico. American Museum Novitates 3815, 1–14.
Kolotl, n. gen. (Scorpiones: Diplocentridae), a new scorpion genus from Mexico.CrossRef | open url image1

Schliep, K. P. (2011). phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593.
phangorn: phylogenetic analysis in R.CrossRef | 1:CAS:528:DC%2BC3MXitVWhur0%3D&md5=7aaf8895eb295cfda4538ba52b3d0ca3CAS | open url image1

Sharma, P. P., Fernández, R., Esposito, L. A., González-Santillán, E., and Monod, L. (2015). Phylogenomic resolution of scorpions reveals multilevel discordance with morphological phylogenetic signal. Proceedings of the Royal Society B 282, 20142953.
Phylogenomic resolution of scorpions reveals multilevel discordance with morphological phylogenetic signal.CrossRef | open url image1

Sissom, W. D. (1994). Descriptions of new and poorly known scorpions of Yemen (Scorpiones: Buthidae, Diplocentridae, Scorpionidae). Fauna of Saudi Arabia 14, 3–39. open url image1

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.CrossRef | 1:CAS:528:DC%2BC2cXmvFCjsbc%3D&md5=dbe02a1b9e110b233409dd1d5b71d108CAS | open url image1

Volschenk, E. S., and Prendini, L. (2008). Aops oncodactylus, gen. et sp. nov., the first troglobitic urodacid (Urodacidae: Scorpiones), with a re-assessment of cavernicolous, troglobitic and troglomorphic scorpions. Invertebrate Systematics 22, 235–257.
Aops oncodactylus, gen. et sp. nov., the first troglobitic urodacid (Urodacidae: Scorpiones), with a re-assessment of cavernicolous, troglobitic and troglomorphic scorpions.CrossRef | open url image1

Vrancken, B., Lemey, P., Rambaut, A., Bedford, T., Longdon, B., Günthard, H. F., and Suchard, M. A. (2015). Simultaneously estimating evolutionary history and repeated traits phylogenetic signal: applications to viral and host phenotypic evolution. Methods in Ecology and Evolution 6, 67–82.
Simultaneously estimating evolutionary history and repeated traits phylogenetic signal: applications to viral and host phenotypic evolution.CrossRef | open url image1



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