Finding hot singles: matching males to females in dimorphic spiders (Araneidae : Micrathena) using phylogenetic placement and DNA barcoding
Ivan L. F. Magalhaes A B D , Pedro H. Martins B , André A. Nogueira C and Adalberto J. Santos B
+ Author Affiliations
- Author Affiliations
A División Aracnología, Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ – CONICET, Av. Ángel Gallardo 470, C1405DJR, Buenos Aires, Argentina.
B Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, CEP 31270-901, Belo Horizonte, Minas Gerais, Brazil.
C Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, n. 321, CEP 05508-900, São Paulo, São Paulo, Brazil.
D Corresponding author. Email: magalhaes@macn.gov.ar
Invertebrate Systematics 31(1) 8-36 https://doi.org/10.1071/IS15062
Submitted: 18 December 2015 Accepted: 17 June 2016 Published: 16 March 2017
Abstract
Many orb-weaving spiders exhibit remarkable sexual dimorphism, hampering the matching of males and females in taxonomic studies. This is the case for the spiny Micrathena spiders, a species-rich Neotropical genus with 27% of its species known from a single sex. In this paper we document several undescribed Micrathena specimens, and test whether they belong to some of those incompletely known species. In order to do so, we: (1) tested the phylogenetic position of males and their putative females using a previous morphological dataset; (2) calculated genetic distances among individuals based on a fragment of the mitochondrial gene cytochrome c oxidase subunit I; and (3) examined their geographical distributions. These approaches, isolated or in combination, allowed us to identify and describe the previously unknown males of M. embira Levi, M. reimoseri Mello-Leitão, M. exlinae Levi, M. miles Simon, M. spinulata F.O. Pickard-Cambridge, M. yanomami Magalhães & Santos and M. cornuta (Taczanowski), and the female of M. beta di Caporiacco. We found that the males previously associated with M. bicolor (Keyserling), M. cornuta and M. lata Chickering had been incorrectly matched with females. The latter actually belongs to a hitherto unnamed species, herein described as Micrathena perfida, sp. nov. New geographical data are given for these and other Micrathena species. Our study highlights the importance of using different sources of data for matching the sexes in diverse groups with strong sexual dimorphism.
Additional keywords: Araneae, cladistics, taxonomy.
References
Alvarez-Padilla Laboratory (2014). ‘Araneomorphae of Mexico, a Digital Images Catalog v2.0. Facultad de Ciencias UNAM.’ Available at: www.unamfcaracnolab.com (Accessed 6 December 2014).Argañaraz, C. I., and Rubio, G. D. (2011). The spider Micrathena shealsi Chickering, 1960 (Araneae: Araneidae): description of the male, with new data on its geographic distribution. Zootaxa 3104, 52–58.
Barone, M. L., Werenkraut, V., and Ramírez, M. J. (2016). New species and phylogenetic relationships of the spider genus Coptoprepes using morphological and sequence data (Araneae: Anyphaenidae). Zootaxa 4175, 436–448.
Barrett, D. H. R., and Hebert, P. D. N. (2005). Identifying spiders through DNA barcodes. Canadian Journal of Zoology 83, 481–491.
| Identifying spiders through DNA barcodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsFylsrk%3D&md5=b10125dda9e2a5563335cb994154d446CAS |
Brignoli, P. (1983). ‘A Catalogue of the Araneae Described Between 1940 and 1981.’ (Manchester University Press: Manchester, England.)
Cheng, R.-C., and Kuntner, M. (2015). Disentangling the size and shape components of sexual dimorphism. Evolutionary Biology 42, 223–234.
| Disentangling the size and shape components of sexual dimorphism.Crossref | GoogleScholarGoogle Scholar |
Chickering, A. M. (1960). Three new species of Micrathena from South America. Breviora 121, 1–11.
Chickering, A. M. (1961). The genus Micrathena (Araneae, Argiopidae) in Central America. Bulletin of the Museum of Comparative Zoology 125, 391–470.
Clouse, R. M., and Wheeler, W. C. (2014). Descriptions of two new, cryptic species of Metasiro (Arachnida: Opiliones: Cyphophthalmi: Neogoveidae) from South Carolina, USA, including a discussion of mitochondrial mutation rates. Zootaxa 3814, 177–201.
| Descriptions of two new, cryptic species of Metasiro (Arachnida: Opiliones: Cyphophthalmi: Neogoveidae) from South Carolina, USA, including a discussion of mitochondrial mutation rates.Crossref | GoogleScholarGoogle Scholar |
di Caporiacco, L. (1947). Diagnosi preliminari de specie nuove di aracnidi della Guiana Brittanica raccolte dai professori Beccari e Romiti. Monitore Zoologico Italiano 56, 20–34.
di Caporiacco, L. (1948). Arachnida of British Guiana collected in 1931 and 1936 by professors Beccari and Romiti. Proceedings of the Zoological Society of London 118, 607–747.
| Arachnida of British Guiana collected in 1931 and 1936 by professors Beccari and Romiti.Crossref | GoogleScholarGoogle Scholar |
Dierkens, M. (2011). Contribution à l’étude des Araneidae de la Guyane Française I: Gasteracanthinae. Les Cahiers du Musée des Confluences – Études Scientifiques 2, 99–108.
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 |
Edwards, G. B. (2013). A philosophy and methodology for matching opposite sexes of one species, exemplified by a new synonym in Myrmarachne (Araneae: Salticidae). Peckhamia 111, 1–12.
Faynel, C., Busby, R. C., and Robbins, R. K. (2012). Review of the species level taxonomy of the neotropical butterfly genus Oenomaus (Lycaenidae, Theclinae, Eumaeini). ZooKeys 222, 11–45.
| Review of the species level taxonomy of the neotropical butterfly genus Oenomaus (Lycaenidae, Theclinae, Eumaeini).Crossref | GoogleScholarGoogle Scholar |
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=301bf4945988b7429a8e829133746d39CAS |
Gilbert, C. C., Frost, S. R., and Strait, D. S. (2009). Allometry, sexual dimorphism, and phylogeny: a cladistic analysis of extant African papionins using craniodental data. Journal of Human Evolution 57, 298–320.
| Allometry, sexual dimorphism, and phylogeny: a cladistic analysis of extant African papionins using craniodental data.Crossref | GoogleScholarGoogle Scholar |
Goloboff, P. A. (1993). Estimating character weights during tree search. Cladistics 9, 83–91.
| Estimating character weights during tree search.Crossref | GoogleScholarGoogle Scholar |
Goloboff, P. A., Farris, J. S., Källersjö, M., Oxelman, B., Ramírez, M. J., 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 |
Hedin, M. C. (1997). Molecular phylogenetics at the population/species interface in cave spiders of the southern Appalachians (Araneae: Nesticidae: Nesticus). Molecular Biology and Evolution 14, 309–324.
| Molecular phylogenetics at the population/species interface in cave spiders of the southern Appalachians (Araneae: Nesticidae: Nesticus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhslSjsLY%3D&md5=336726cb7d47a0209da912e3b52896a2CAS |
Hedin, M. C., and Maddison, W. P. (2001). A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae). Molecular Phylogenetics and Evolution 18, 386–403.
| A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1ansbg%3D&md5=a38c51da31fc72eaf622438a37abc9efCAS |
Hulcr, J., Miller, S. E., Setliff, G. P., Darrow, K., Mueller, N. D., Hebert, P. D. N., and Weiblen, G. D. (2007). DNA barcoding confirms polyphaghy in a generalist moth Homona mermerodes (Lepidoptera: Tortricidae). Molecular Ecology Notes 7, 549–557.
| DNA barcoding confirms polyphaghy in a generalist moth Homona mermerodes (Lepidoptera: Tortricidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpslOhtbs%3D&md5=6cc782f1b73f99e51a055ef42e1bc668CAS |
Levi, H. W. (1985). The spiny orb-weaver genera Micrathena and Chaetacis (Araneae: Araneidae). Bulletin of the Museum of Comparative Zoology 150, 429–618.
Levi, H. W., and Santos, A. J. (2013). New synonymies and a revalidation in the spider genera Eustala and Micrathena (Araneae: Araneidae). Zoologia 30, 221–226.
| New synonymies and a revalidation in the spider genera Eustala and Micrathena (Araneae: Araneidae).Crossref | GoogleScholarGoogle Scholar |
Magalhães, I. L. F., and Santos, A. J. (2011). Two new species and taxonomic notes on the Neotropical spiny orb-weaving spiders Micrathena and Chaetacis (Araneae: Araneidae), with remarks on the development of Micrathena excavata. Zootaxa 2983, 39–56.
Magalhães, I. L. F., and Santos, A. J. (2012). Phylogenetic analysis of Micrathena and Chaetacis spiders (Araneae: Araneidae) reveals multiple origins of extreme sexual size dimorphism and long abdominal spines. Zoological Journal of the Linnean Society 166, 14–53.
McHugh, A., Yablonsky, C., Binford, G., and Agnarsson, I. (2014). Molecular phylogenetics of Caribbean Micrathena (Araneae: Araneidae) suggests multiple colonization events and single island endemism. Invertebrate Systematics 28, 337–349.
Meier, R., and Lim, G. S. (2009). Conflict, convergent evolution, and the relative importance of immature and adult characters in endopterygote phylogenetics. Annual Review of Entomology 54, 85–104.
| Conflict, convergent evolution, and the relative importance of immature and adult characters in endopterygote phylogenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsFeltg%3D%3D&md5=4e3606e3606d6321f23c7320f4c87015CAS |
Mello-Leitão, C.F. (1930). Aranhas do Cuminá. Archivos do Museu Nacional do Rio de Janeiro 32, 51–75.
Mello-Leitão, C. F. (1935). Three interesting new Brasilian spiders. Revista Chilena de Historia Natural (Valparaiso, Chile) 39, 94–98.
Mello-Leitão, C. F. (1940). Aranhas do Espírito Santo coligidas por Mario Rosa, em 1936 e 1937. Archivos de Zoologia do Estado de São Paulo 2, 199–214.
Miranda, L. S., Collins, E. G., and Marques, A. C. (2010). Molecules clarify a cnidarian life cycle – the “hydrozoan” Microhydrula limopsicola is an early life stage of the staurozoan Haliclystus antarcticus. PLoS One 5, e10182.
| Molecules clarify a cnidarian life cycle – the “hydrozoan” Microhydrula limopsicola is an early life stage of the staurozoan Haliclystus antarcticus.Crossref | GoogleScholarGoogle Scholar |
Nogueira, A. A., Venticinque, E. M., Brescovit, A. D., Lo-Man-Hung, N. F., and Candiani, D. F. (2014). List of species of spiders (Arachnida, Araneae) from the Pico da Neblina, state of Amazonas, Brazil. Check List 10, 1044–1060.
| List of species of spiders (Arachnida, Araneae) from the Pico da Neblina, state of Amazonas, Brazil.Crossref | GoogleScholarGoogle Scholar |
Pickard-Cambridge, O. (1890). Arachnida. Araneida. Biologia Centrali-Americana Zoologia 1, 57–72.
Pickard-Cambridge, F. O. (1904). Arachnida – Araneida and Opiliones. Biologia Centrali-Americana Zoologia 2, 465–560.
Platnick, N. I., and Shadab, M. U. (1978). A review of the spider genus Anapis (Araneae, Anapidae), with a dual cladistic analysis. American Museum Novitates 2663, 1–23.
Przybyłowicz, L., and Tarcz, S. (2015). Strong sexual dimorphism unraveled by DNA analysis – towards a better understanding of Pseudothyretes classification (Lepidoptera: Erebidae: Arctiinae). Zoological Journal of the Linnean Society 173, 22–54.
| Strong sexual dimorphism unraveled by DNA analysis – towards a better understanding of Pseudothyretes classification (Lepidoptera: Erebidae: Arctiinae).Crossref | GoogleScholarGoogle Scholar |
Reimoser, E. (1917). Die Spinnengattung Micrathena Sundevall. Verhandlungen der Kaiserlich-Königlichen Zoologisch-Botanischen Gesellschaft in Wien 67, 73–160.
Sharma, P. P., Clouse, R. M., and Wheeler, W. C. (). Hennig’s semaphoront concept and the use of ontogenetic stages in phylogenetic reconstruction. Cladistics , .
Simon, E. (1895). ‘Histoire Naturelle des Araignées, 1.’ (Paris, Librarie Encyclopédique de Roret: Paris, France.)
Simon, E. (1897). Etudes arachnologiques. 27e mémoire. XLII. Descriptions d’espèces nouvelles de l’ordre des Araneae. Annales de la Société Entomologique de France 65, 465–510.
Soares, B. A. M., and Camargo, H. F. A. (1948). Aranhas coligidas pela Fundação Brasil-Central (Arachnida-Araneae). Boletim do Museu Paraense Emílio Goeldi 10, 355–409.
Steyer, J. S. (2000). Ontogeny and phylogeny in temnospondyls: a new method of analysis. Zoological Journal of the Linnean Society 130, 449–467.
| Ontogeny and phylogeny in temnospondyls: a new method of analysis.Crossref | GoogleScholarGoogle Scholar |
Taczanowski, L. (1873). Les aranéides de la Guyane Française. Horae Societatis Entomologicae Rossicae 9, 113–150, 261–286.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=31e52c88992083420b0597f29824352bCAS |
Tanikawa, A. (2011). The first description of a male of Paraplectana tsushimensis (Araneae: Araneidae). Acta Arachnologica 60, 71–73.
| The first description of a male of Paraplectana tsushimensis (Araneae: Araneidae).Crossref | GoogleScholarGoogle Scholar |
Trivinho-Strixino, S., Pepinelli, M., Siqueira, T., and Roque, F. O. (2012). DNA barcoding of Podonomus (Chironomidae, Podonominae) enables stage association of a named species and reveals hidden diversity in Brazilian inselbergs. Annales de Limnologie – International Journal of Limnology 48, 411–423.
| DNA barcoding of Podonomus (Chironomidae, Podonominae) enables stage association of a named species and reveals hidden diversity in Brazilian inselbergs. Annales de Limnologie – International Crossref | GoogleScholarGoogle Scholar |
Vollrath, F. (1998). Dwarf males. Trends in Ecology & Evolution 13, 159–163.
| Dwarf males.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFyltQ%3D%3D&md5=0b7d37ee9604aa100c7199289af79410CAS |
Wolfe, J. M., and Hegna, T. A. (2014). Testing the phylogenetic position of Cambrian pancrustacean larval fossils by coding ontogenetic stages. Cladistics 30, 366–390.
| Testing the phylogenetic position of Cambrian pancrustacean larval fossils by coding ontogenetic stages.Crossref | GoogleScholarGoogle Scholar |
World Spider Catalog (2016). ‘World Spider Catalog, Version 17.0.’ Natural History Museum Bern. Available at: http://wsc.nmbe.ch (Accessed 15 May 2016).
