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

Molecular phylogeny informs generic and subgeneric concepts in the Schizoptera Fieber genus group (Heteroptera : Schizopteridae) and reveals multiple origins of female-specific elytra

S. Leon A B and C. Weirauch A
+ Author Affiliations
- Author Affiliations

A Department of Entomology, University of California, Riverside, 900 University Avenue, Riverside, CA 92521, USA.

B Corresponding author. Email: sleon002@ucr.edu; sleon@archbold-station.org

Invertebrate Systematics 31(2) 191-207 https://doi.org/10.1071/IS16003
Submitted: 13 January 2016  Accepted: 9 November 2016   Published: 26 April 2017

Abstract

Wing dimorphism occurs in many genera of Schizopteridae Reuter, 1891 and other litter bugs (Heteroptera : Dipsocoromorpha), in both males and females. In the largest litter bug genus, Schizoptera Fieber, and closely related taxa, sexual wing dimorphism is observed in several species whereby males are macropterous, but females possess elytra, or hardened forewings – a feature that is rare outside of beetles and that we here refer to as female-specific elytra. Phylogenetic hypotheses for Schizoptera are unavailable, but are essential to reveal if female-specific elytra evolved once or multiple times within the genus and to test if the presence of elytra can reverse states to macropterous wings. In addition, generic and subgeneric concepts of this speciose genus-group have not been tested in a phylogenetic framework, and relationships with other schizopterid genera remain largely unknown. Our molecular phylogeny of Schizoptera and related genera documents that this genus is currently polyphyletic, and we raise the subgenus Kophaegis to generic rank to render Schizoptera monophyletic (Orthorhagus was recently elevated to genus). Relationships within Schizoptera reveal several well supported clades, some of them corresponding to currently recognised subgenera. To examine the value of previously used diagnostic features, we optimise 11 morphological characters on the molecular phylogeny and update generic and subgeneric diagnoses. Tracing transitions between macropterous and elytrous wing types, we show that female-specific elytra evolved at least seven times within Schizopteridae, four of those times within the Schizoptera genus-group, and that elytra reversed to macropterous wings at least twice. We propose that Schizopteridae may be an excellent model to study the selective pressures that have given rise to sexually dimorphic traits.

Additional keywords: ancestral state reconstruction, evolution, Schizopteridae, wing dimorphisms.


References

Alexander, R. D. (1968). Life cycle origins, speciation, and related phenomena in crickets. The Quarterly Review of Biology 43, 1–41.
Life cycle origins, speciation, and related phenomena in crickets.CrossRef | 1:STN:280:DyaF1c3nsl2lsw%3D%3D&md5=195828842b145c3367ef4b1432a2fdbaCAS |

Andersen, N. M. (1993). The evolution of wing polymorphism in water striders (Gerridae): a phylogenetic approach. Oikos 67, 433–443.
The evolution of wing polymorphism in water striders (Gerridae): a phylogenetic approach.CrossRef |

Aukema, B. (1995). The evolutionary significance of wing dimorphism in carabid beetles (Coleoptera: Carabidae). Researches on Population Ecology 37, 105–110.
The evolutionary significance of wing dimorphism in carabid beetles (Coleoptera: Carabidae).CrossRef |

Beutel, R. G., and Gorb, S. (2001). Ultrastructure of attachment specializations of hexapods (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny. Journal of Zoological Systematics and Evolutionary Research 39, 177–207.
Ultrastructure of attachment specializations of hexapods (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny.CrossRef |

Braendle, C., Davis, G. K., Brisson, J. A., and Stern, D. L. (2006). Wing dimorphism in aphids. Heredity 97, 192–199.
Wing dimorphism in aphids.CrossRef | 1:STN:280:DC%2BD28rgsVegsw%3D%3D&md5=2067ce5b3ed90ddb4d436671e4939bcfCAS |

Denno, R. F. (1994). The evolution of dispersal polymorphisms in insects: the influence of habitats, host plants and mates. Researches on Population Ecology 36, 127–135.
The evolution of dispersal polymorphisms in insects: the influence of habitats, host plants and mates.CrossRef |

Denno, R. F., Douglas, L. W., and Jacobs, D. (1985). Crowding and host plant nutrition: environmental determinants of wing-form in Prokelisia marginata. Ecology 66, 1588–1596.
Crowding and host plant nutrition: environmental determinants of wing-form in Prokelisia marginata.CrossRef |

Desender, K. (1987). Distribution, the special case of sex-linked wing dimorphism and phenology of the life cycle in Trichotichnus laevicollis and T. nitens (Coleoptera: Carabidae). Deutsche Entomologische Zeitschrift 34, 77–84.
Distribution, the special case of sex-linked wing dimorphism and phenology of the life cycle in Trichotichnus laevicollis and T. nitens (Coleoptera: Carabidae).CrossRef |

Emsley, M. G. (1969). The Schizopteridae (Hemiptera: Heteroptera) with the descriptions of new species from Trinidad. Memoirs of the American Entomological Society 25, 1–154.

Esaki, T., and Miyamoto, S. (1959). A new or little known Hypselosoma from Amami-Oshima and Japan, with the proposal of a new tribe for the genus (Hemiptera). Seibolda Fukuoka 2, 109–120.

Farris, J. S., Albert, V. A., Källersjö, M., Lipscomb, D., and Kluge, A. G. (1996). Parsimony jackknifing outperforms neighbor-joining. Cladistics 12, 99–124.
Parsimony jackknifing outperforms neighbor-joining.CrossRef |

Fieber, F. X. (1860). Exegesen in Hemipteren. Wiener Entomologische Monatschrift 9, 257–272.

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=301bf4945988b7429a8e829133746d39CAS |

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 |

Guerra, P. A. (2011). Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis. Biological Reviews of the Cambridge Philosophical Society 86, 813–835.
Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis.CrossRef |

Harrison, R. G. (1980). Dispersal polymorphisms in insects. Annual Review of Ecology and Systematics 11, 95–118.
Dispersal polymorphisms in insects.CrossRef |

Heidemann, O. (1906). A new genus and species of hemipterous family Ceratocombidae from the United States. Proceedings of the Entomological Society of Washington DC 7, 192–194.

Honěk, A. (1995). Factors and consequences of a non-functional alary polymorphism in Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae). Researches on Population Ecology 37, 111–118.
Factors and consequences of a non-functional alary polymorphism in Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae).CrossRef |

Karlsson Green, K. K., Kovalev, A., Svensson, E. I., and Gorb, S. N. (2013). Male clasping ability, female polymorphism and sexual conflict: fine-scale elytral morphology as a sexually antagonistic adaptation in female diving beetles. Journal of the Royal Society, Interface 10, 20130409.
Male clasping ability, female polymorphism and sexual conflict: fine-scale elytral morphology as a sexually antagonistic adaptation in female diving beetles.CrossRef |

Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518.
MAFFT version 5: improvement in accuracy of multiple sequence alignment.CrossRef | 1:CAS:528:DC%2BD2MXhtV2qsbc%3D&md5=b094173d597c027ec1356c22e6d99299CAS |

Knyshov, A., Leon, S., Hoey-Chamberlain, R., and Weirauch, C. (2016). Pegs, pouches and spines: systematics and comparative morphology of the new world genus Chinannus Wygodzinsky, 1948. In ‘Thomas Say Monographs, Vol. 35’. (Ed. J. Wooley.) pp. 1–112. (Entomological Society of America: Annapolis, MD.)

Langellotto, G. A., Denno, R. F., and Ott, J. R. (2000). A trade-off between flight capability and reproduction in males of a wing-dimorphic insect. Ecology 81, 865–875.
A trade-off between flight capability and reproduction in males of a wing-dimorphic insect.CrossRef |

Lawrence, J. F., and Newton, A. F. (1982). Evolution and classification of beetles. Annual Review of Ecology and Systematics 13, 261–290.
Evolution and classification of beetles.CrossRef |

Leon, S., and Weirauch, C. (2016a). Small bugs, big changes: taxonomic revision of Orthorhagus McAtee & Malloch. Neotropical Entomology 45, 559–572.
Small bugs, big changes: taxonomic revision of Orthorhagus McAtee & Malloch.CrossRef | 1:STN:280:DC%2BC2s%2FosFSrsw%3D%3D&md5=05747bba86721df655f37325779f4980CAS |

Leon, S., and Weirauch, C. (2016b). Scratching the surface? Taxonomic revision of the subgenus (Odontorhagus) reveals vast undocumented biodiversity in the largest litter bug genus Schizoptera Fieber (Hemiptera: Dipsocoromorpha). Zootaxa 4184, 255–284.
Scratching the surface? Taxonomic revision of the subgenus (Odontorhagus) reveals vast undocumented biodiversity in the largest litter bug genus Schizoptera Fieber (Hemiptera: Dipsocoromorpha).CrossRef |

Masaki, S., and Oyama, N. (1963). Photoperiodic control of growth and wing-form in Nemobius yezoensis (Orthoptera  : Gryllidae). Japanese Journal of Entomology 31, 16–26.

McAtee, W. L., and Malloch, J. R. (1925). Revision of bugs of the family Cryptostemmatidae in the collection of the United States National Museum. Proceedings of the United States National Museum 67, 1–153.
Revision of bugs of the family Cryptostemmatidae in the collection of the United States National Museum.CrossRef |

McFarlane, J. E. (1962). Effect of diet and temperature on wing development in Grylloides sigillatus (Walker). Annales de la Société Entomologique du Québec 7, 28–33.

Miller, K. B. (2003). The phylogeny of diving beetles (Coleoptera: Dytiscidae) and the evolution of sexual conflict. Biological Journal of the Linnean Society. Linnean Society of London 79, 359–388.
The phylogeny of diving beetles (Coleoptera: Dytiscidae) and the evolution of sexual conflict.CrossRef |

Müller, C. B., Williams, I. S., and Hardie, J. (2001). The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology 26, 330–340.
The role of nutrition, crowding and interspecific interactions in the development of winged aphids.CrossRef |

O’Donnell, J. E. (1991). A new coleopteroid Lethaeine from Southern South America (Hemiptera: Lygaeidae: Rhyparochrominae). Journal of the New York Entomological Society 99, 87–96.

Philips, T. K. (2000). Phylogenetic analysis of the New World Ptininae (Coleoptera: Bostrichoidea). Systematic Entomology 25, 235–262.
Phylogenetic analysis of the New World Ptininae (Coleoptera: Bostrichoidea).CrossRef |

Poinar, G. J., and Brown, A. (2014). New genera and species of jumping ground bugs (Hemiptera: Schizopteridae) in Dominican and Burmese amber, with a description of a meloid (Coleoptera: Meloidae) triungulin on a Burmese specimen. Annales de La Société Entomologique de France (N.S.) 50, 372–381.

Poppius, B. (1910). Neue Ceratocombiden. Ofversigt Af Finska Vetenskapssocietetens Forhandlingar Helsingfors 52, 1–14.

Prendini, L., Weygoldt, P., and Wheeler, W. C. (2005). Systematics of Damon variegatus group of African whip spiders (Chelicerata: Amblypygi): evidence from behavior, morphology and DNA. Organisms, Diversity & Evolution 5, 203–236.
Systematics of Damon variegatus group of African whip spiders (Chelicerata: Amblypygi): evidence from behavior, morphology and DNA.CrossRef |

Redéi, D. (2008). First record of Pinochius Carayon, 1949 from the Oriental Region, with description of a new species from Vietnam (Heteroptera: Schizopteridae). In ‘Advances in Heteroptera Research: Festschrift in Honour of 80th Anniversary of Michail Josifov’. (Eds S. Grozeva and N. Simov Simov.) pp. 327–337. (Pensoft: Sofia, Bulgaria.)

Reuter, O. M. (1882). Sur le genre Schizoptera Fieb. Revue d’Entomologie 1, 162–164.

Reuter, O. M. (1891). Monographia Ceratocombidarum orbis terrestris. Acta Societatis Scientiarum Fennicae 19, 1–28.

Roff, D. A. (1986). The evolution of wing dimorphism in insects. Evolution 40, 1009–1020.
The evolution of wing dimorphism in insects.CrossRef |

Schwendinger, P. J., and Giribet, G. (2005). The systematics of the Southeast Asian genus Fangensis Rambla (Opiliones: Cyphophthalmi: Stylocellidae). Invertebrate Systematics 19, 297–323.
The systematics of the Southeast Asian genus Fangensis Rambla (Opiliones: Cyphophthalmi: Stylocellidae).CrossRef |

Slater, J. A. (1975). On the biology and zoogeography of Australian Lygaeidae (Hemiptera: Heteroptera) with special reference to the southwest fauna. Australian Journal of Entomology 14, 47–64.
On the biology and zoogeography of Australian Lygaeidae (Hemiptera: Heteroptera) with special reference to the southwest fauna.CrossRef |

Slater, J. A. (1977). The incidence and evolutionary significance of wing polymorphisms in lygaeid bugs with particular reference to those of South Africa. Biotropica 9, 217–229.
The incidence and evolutionary significance of wing polymorphisms in lygaeid bugs with particular reference to those of South Africa.CrossRef |

Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.CrossRef | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=c868f257e775d7586364223c6888c21aCAS |

Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology 57, 758–771.
A rapid bootstrap algorithm for the RAxML Web servers.CrossRef |

Štys, P. (1975). Redescription of Ptenidiophyes mirabilis Reuter (Heteroptera: Schizopteridae). Vestník Čekoslovenské Společnosti Zoologické 39, 154–159.

Svensson, E. I., Abbott, J. K., Gosden, T. P., and Coreau, A. (2009). Female polymorphisms, sexual conflict and limits to speciation processes in animals. Evolutionary Ecology 23, 93–108.
Female polymorphisms, sexual conflict and limits to speciation processes in animals.CrossRef |

Sweet, M. H. (1964). The biology and ecology of the Rhyparochrominae of New England. Entomologica Americana 43, 1–124.

Thayer, M. K. (1992). Discovery of sexual wing dimorphism in Staphylinidae (Coleoptera): “Omaliumflavidum and a discussion of wing dimorphisms in insects. Journal of the New York Entomological Society 100, 540–573.

Vaidya, G., Lohman, D. J., and Meier, R. (2011). SequeneMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171–180.
SequeneMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information.CrossRef |

Weirauch, C. (2012). Voragocoris schuhi a new genus and species of Neotropical Schizopterinae (Hemiptera: Heteroptera: Schizopteridae). Entomologica Americana 118, 285–294.
Voragocoris schuhi a new genus and species of Neotropical Schizopterinae (Hemiptera: Heteroptera: Schizopteridae).CrossRef |

Weirauch, C., and Frankenberg, S. (2015). From “insect soup” to biodiversity discovery: taxonomic revision of Peloridinannus Wygodzinksy, 1951 (Hemiptera: Schizopteridae), with description of six new species. Arthropod Systematics & Phylogeny 73, 457–471.

Weirauch, C., and Munro, J. B. (2009). Molecular phylogeny of the assassin bugs (Hemiptera: reduviidae), based on mitochondrial and nuclear ribosomal genes. Molecular Phylogenetics and Evolution 53, 287–299.
Molecular phylogeny of the assassin bugs (Hemiptera: reduviidae), based on mitochondrial and nuclear ribosomal genes.CrossRef | 1:CAS:528:DC%2BD1MXptlyksbc%3D&md5=14ef355563f37d0299f20556f4fa35aaCAS |

Weirauch, C., and Štys, P. (2014). Litter bugs exposed: phylogenetic relationships of Dipsocoromorpha (Hemiptera: Heteroptera) based on molecular data. Insect Systematics & Evolution 45, 351–370.
Litter bugs exposed: phylogenetic relationships of Dipsocoromorpha (Hemiptera: Heteroptera) based on molecular data.CrossRef |

Zera, A. J., and Denno, R. F. (1997). Physiology and ecology of dispersal polymorphism in insects. Annual Review of Entomology 42, 207–230.
Physiology and ecology of dispersal polymorphism in insects.CrossRef | 1:CAS:528:DyaK2sXjvFSlug%3D%3D&md5=3491c872a336429a86c1ccf4aea3a46eCAS |



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