Intersexuality in the holotype of Photina gracilis (Mantodea: Mantidae: Photininae) and its taxonomic implications

SHORT COMMUNICATION

Intersexuality in the holotype of Photina gracilis (Mantodea: Mantidae: Photininae) and its taxonomic implications

Antonio A. Agudelo R.

Programa de Pós-graduação em Entomologia, Instituto Nacional de Pesquisas da Amazônia. Avenida André Araujo 2936, Aleixo, 69060-001 Manaus, AM, Brazil. E mail: [e-mail]

ABSTRACT

Parasitism by horsehair worms (Nematomorpha) in Mantodea is well known, but only a few cases of intersexuality were reported in the literature. In the present study, intersexuality of the holotype of Photina gracilis Giglio-Tos, 1915 is documented as a possible consequence of nematomorph parasitism. Photina gracilis and Photina laevis Giglio-Tos, 1915 are established as new subjective junior synonyms of Photina vitrea (Burmeister, 1838). The female holotype of Mantis (Cardioptera) gymnopyga Burmeister, 1838, which was associated and synonymized with P. vitrea, is recognized as a member of the genus Coptopteryx and the combination Coptopteryx gymnopyga (Burmeister, 1838) is revalidated. The substitute name Photina gymnopyga (Burmeister, 1838), instead of Mantis (Photina) vitrea Burmeister, 1838 (nec Mantis vitrea Stoll, 1813), is discarded and established as a new synonym of Coptopteryx gymnopyga. The name vitrea Burmeister, 1838 must be maintained until ruling by the International Commission on Zoological Nomenclature.

Keywords: Coptopteryx; Nematomorpha; parasitism; Photina; praying mantises.

In nature, individuals do not always show a clearly defined sexual dimorphism. When there is no morphological differentiation between male and female the organisms are usually called gynandromorphs or intersexes and, in many cases, the choice is arbitrary (Narita et al. 2010). Intersexuality has been documented for several groups of Arthropoda. Narita et al. (2010) reviewed many cases of gynandromorphism and intersexuality in arthropods and commented on the meaning and differences between these terms. In Hexapoda, the occurrence of individuals having both male and female phenotypes is supported by numerous references, especially in Coleoptera (Vasko 2008), Diptera (Schutt & Nöthiger 2000), Hymenoptera (Pereira et al. 2003), Lepidoptera (Kusnezov 1926), and Orthoptera (Cappe De Baillon 1924). As it might be expected, the most studied organisms when sexual development is concerned are in Drosophila (Diptera) (Schutt & Nöthiger 2000), which have served as a paradigm for understanding the mechanisms of sexual differentiation, at least in Hexapoda. There are few reported cases of sexual phenotypic combinations in Mantodea individuals: Roy (2003) reported intersexuality in individuals of Prohierodula Bolívar, 1908 (Mantidae), and Lombardo & Umbriaco (2011) in the holotype of Parastagmatoptera abnormis Beier, 1963 (Mantidae). In both cases, intersexuality was associated with parasitism by nematomorphs. Bèthoux (2010) presented a particular case of "feminization" as a result of alteration in the organization of a developmental module in Creobroter gemmatus (Stoll, 1813) (Hymenopodidae), and treated it as a case of mixed gynandromorphy.

As part of an ongoing review of the types of Neotropical Mantodea in the main entomological collections and museums of Europe, particularly the types of Photininae, I found three cases of intersexuality. The first had been previously reported by Lombardo & Umbriaco (2011) in the holotype of P. abnormis, which is deposited in the Biozentrum Grindel und Zoologisches Museum (ZMH, Hamburg, Germany). In the same work, P. abnormis was considered a junior synonym of Parastagmatoptera flavoguttata (Serville, 1839). The second case pertains the holotype of Mantis longicornis Charpentier, 1841 (Mantidae) (Fig. 1), which was synonymized by Saussure (1871) with Photina vitrea (Burmeister, 1838); the specimen is deposited in the Museum für Naturkunde der Humboldt Universität, Berlin (MNHB), and is labeled as a female, but it is likely a feminized male with some female characteristics, for instance short wings; unfortunately, the abdomen of this specimen is lost, which does not allow associating intersexuality with parasitic induction. The third case was discovered in the holotype of Photina gracilis Giglio-Tos, 1915 (Fig. 2), also deposited in the MNHB, which required the detailed re-evaluation of its taxonomic status presented here.

The holotype of P. gracilis from the old colonial village of Teresópolis, currently municipality of Águas Mornas in the state of Santa Catarina, Brazil, is well preserved. The interpretation of Giglio-Tos (1915) that it is a distinctive "female" of Photina may be justifiable, since the general habitus of the holotype, under the naked eye, is that of a typical female of the genus. However, a careful examination of the posterior part of the abdomen revealed the developed external male genitalia. I had the opportunity to dissect the external genitalia of the holotype in order to compare with the male genitalia of the type species of Photina (Fig. 4).

The external male genitalia of P. gracilis (Fig. 5) are similar to the genitalia of the holotype of Mantis (Photina) vitrea Burmeister, 1838 (now Photina vitrea), which allows the conclusion that the holotype of P. gracilis is a feminized form of P. vitrea. In addition, the external black color of the set of posteroventral spines of the forefemora is a distinctive characteristic present in both specimens, and which helps to demonstrate their conspecific status. Giglio-Tos (1915) also described another Photina female under the name Photina laevis Giglio-Tos, 1915 (Fig. 3) from the same locality of P. gracilis, and argued that the "female" of P. gracilis differed from P. laevis by its smaller size and the size of the mesothoracic wings. The observation of the female holotype of P. laevis deposited at MNHB allows me to infer that the features used by Giglio-Tos (1915) to distinguish P. laevis from P. gracilis are just a product of the feminization of the intersexed holotype of P. gracilis. Therefore, P. gracilis and P. laevis are hereby established as new junior synonyms of P. vitrea. I also compared P. gracilis with the holotype of Mantis (Cardioptera) gymnopyga Burmeister, 1838 from the questionable locality of Pará (Brazil), deposited in MNHB (Fig. 6), which was treated as the female of P. vitrea by Charpentier (1841). The female type of M. (C.) gymnopyga is clearly a representative of Coptopteryx. However, the possibility that M. (C.) gymnopyga is a junior synonym of the original nominal species of Coptopteryx was ruled out, because M. (C.) gymnopyga was described before the other species of Coptopteryx and thus has priority over other available names (ICZN principle of priority, art. 23), whereby the suggestion of Kirby (1904) to use the combination Coptopteryx gymnopyga (Burmeister, 1838) should be revalidated. Therefore, the suggestion of Koçak & Kemal (2008) to use the substitute combination Photina gymnopyga (Burmeister) instead of Mantis (Photina) vitrea Burmeister, 1838, nec Mantis vitrea Stoll, 1813, should be discarded (ICZN, art. 60.2.1) and established as a new synonym of Coptopteryx gymnopyga. The possible homonymy of Mantis (Photina) vitrea and Mantis vitrea is being reviewed by the International Commission on Zoological Nomenclature (Case 3402, ICZN 2007). The Commission was asked to use its plenary powers to place the name vitrea Burmeister, 1838 on the official list of specific names in Zoology with the endorsement that it is not invalid (Svenson & Branham 2007). The case 3402 is awaiting a decision from the commission. While the case is under consideration, the use of the junior name (vitrea Burmeister, 1838) is to be maintained (ICZN, art. 82).

After dissecting the external genitalia of P. gracilis I discovered a nematomorph specimen inside its abdomen, which protruded between the supranal and subgenital plates (Fig. 7). This suggests that the intersexuality of the type specimen of P. gracilis was influenced by the presence of the nematomorph, as in the case of P. abnormis and Prohierodula (Roy 2003, Lombardo & Umbriaco 2011). Although there are only a few cases of intersexuality in Mantodea, the records of parasitism caused by Nematomorpha, especially by members of the horsehair worms of the genus Chordodes Creplin, 1847, were well documented by Schmidt-Rhaesa & Ehrmann (2001). These nematomorphs seldom kill their hosts, but usually reduce their reproductive capacity (Welch 1965) and have the ability to interfere in the differentiation of sexual characters, acting as one of the main epigenetic factors of intersexuality in Insecta (Wülker 1975). Although Wülker (1975) suggested some mechanism of parasitic primary influence, the regulation and process of how the parasitism becomes an intersexual phenotypic expression in the host are not well understood.

Summary of the nomenclatural acts in this paper. Photina gracilis Giglio-Tos, 1915 and Photina laevis Giglio-Tos, 1915 are subjective junior synonyms of Photina vitrea (Burmeister, 1838) (ICNZ, art. 23). The substitute name Photina gymnopyga (Burmeister, 1838), instead of Mantis (Photina) vitrea Burmeister, 1838 (nec Mantis vitrea Stoll, 1813), suggested by Koçak & Kemal (2008), is discarded (ICZN, art. 60.2.1) and established as a new synonym of Coptopteryx gymnopyga (Burmeister, 1838), combination suggested by Kirby (1904). The name vitrea Burmeister, 1838 must be maintained until the commission ruling (ICZN, art. 82).

ACKNOWLEDGMENTS

This research was financed with resources from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) through a doctoral scholarship (process number 156567/2010-5). I'm indebted to Michael Ohl (MNHB) and his institution for granting access to the entomological collection. My sincere thanks once again to José A. Rafael (INPA) for the continued support.

LITERATURE CITED

Submitted: 12.II.2014

Accepted: 06.VI.2014

• Béthoux, O. 2010. Alteration of sex-related developmental modules: A case of "feminized" male wing morphology in Creobroter gemmatus (Mantodea: Hymenopodidae). European Journal of Entomology 107: 133-135.
• Cappe De Baillon, P. 1924. Recherches sur le gynandromorphism. Metrioptera brachyptera L. et Leptophyes punctatissima Bosc. La Cellule 34: 69-132.
• Charpentier, T.V. 1841. VII-Einige Bemerkungen die Orthopteren betreffend, besonders in Bezug auf Burmeister's und Serville's Schriften über diese Insektenabtheilung. Zeitschrift für die Entomologie 3 (1/2): 283-305.
• Giglio-Tos, E. 1915. Mantidi esotici. Generi e specie nuove. Bulletino della Società Entomologica Italiana 46: 31-108.
• ICZN. 2007. Current Cases and list of available names, Case 3402. International Commission on Zoological Nomenclature, available on line at: http://iczn.org/simpletaxonomy/term/164 [Accessed: 19/VIII/2014]
• Kirby, W.F. 1904. A synonymic Catalogue of Orthoptera. (Forficulidae, Hemimeridae, Blattidae, Mantidae and Phasmidae). London, British Museum, Natural History, vol. 1, I-X+501p.
• Koçak, A. & M. Kemal. 2008. Miscellaneous nomenclatural notes. Miscellaneous Papers, Centre for Entomological Studies Ankara 145: 1-12.
• Kusnezov, N.J. 1926. The morphology of the copulatory structures in some cases of gynandromorphism in Lepidoptera. Biological Bulletin 51: 245-256.
• Lombardo, F. & R. Umbriaco. 2011. Taxonomic re-evaluation of Parastagmatoptera abnormis Beier, 1963 (Dictyoptera, Mantidae: Stagmatopterinae): An unusual case of "parasite-induced" synonymy. Zootaxa 2735: 31-34.
• Narita, S.; R. Pereira; F. Kejlleberg & D. Kageyama. 2010. Gynandromorphs and intersexes: potential to understand the mechanism of sex determination in arthropods. Terrestrial Arthropod Reviews 3: 63-96.
• Pereira, R.A.S.; A.P. Prado & F. Kjellberg. 2003. Gynandromorphism in pollinating fig wasps (Hymenoptera: Agaonidae). Entomological News 114: 152-155.
• Roy, R. 2003. A propos de deux males parasites de Prohierodula Bolivar, 1908 (Dictyoptera, Mantidae). Bulletin de la Société entomologique de France 108: 181-183.
• Saussure, H. de. 1871. Synopsis des Mantides Américains. In: Memories pour servir a L'Histoire Naturelle du Mexique, des Antilles et États-Unis. Genève et Bale, H. George, 4ª Mem., 186p.
• Schmidt-Rhaesa, A. & R. Ehrmann. 2001. Horsehair worms (Nematomorpha) as parasites of praying mantids with a discussion of their life cycle. Zoologischer Anzeiger 240: 167-179.
• Schutt, C. & R. Nothiger. 2000. Structure, function and evolution of sex-determining systems in dipteran insects. Development 127: 667-677.
• Svenson, G. & M. Branham. 2007. Case 3402. Photinini LeConte, 1881 (Insecta, Coleoptera) and Photininae Giglio-Tos, 1915 (Insecta, Mantodea): proposed resolution of homonymy between family-group names. Bulletin of Zoological Nomenclature 64 (4): 243-251.
• Vasko, B. 2008. Occurrences of teratosus [teratosis] and gynandromorphism among some species of beetles of the genus Polyphylla (Coleoptera, Melolonthidae). Vestnik Zoologii 42: 221-227.
• Welch, H. E. 1965. Entomophilic Nematode. Annual Review of Entomology 10: 275-302.
• Wülker, W. 1975. Parasite-induced castration and intersexuality in insects, p. 121-134. In: R. Reinboth (Ed). Intersexuality in the animal kingdom. New York, Springer-Verlag, 449p.

Publication Dates

• Publication in this collection
  08 Sept 2014
• Date of issue
  Aug 2014

History

• Accepted
  06 June 2014
• Received
  12 Feb 2014