Abstract
Peckia is the most species-rich necrophagous genus among the Neotropical sarcophagids, encompassing 67 species distributed in 5 subgenera. Recent phylogenetic studies have challenged the monophyly of this genus with regard to species of the genera Peckiamyia, Titanogrypa, and Villegasia, and the genera Engelimyia, Helicobia, Retrocitomyia, and Sarcophaga. These genera have variously been hypothesized as sister groups to Peckia, or genera closely related to it. We applied cladistic methods using both molecular and morphological data to study phylogenetic relationships of these mostly necrophagous taxa. All currently recognized species of Peckia were included in our analysis. Based on 116 morphological characters and sequences of five gene fragments, we corroborate the recent division of Peckia into five subgenera, and we argue that the reduction of the acrophallic median stylus is an autapomorphic condition supporting the clade (Peckia + (Lipoptilocnema (Helicobia + Sarcophaga))). Our analysis shows that Peckiamyia is sister to Retrocitomyia, and Titanogrypa is sister to Villegasia, which together with Engelimyia form lineages that emerge in a basal divergence with regard to the clade with no median stylus. Alternative homology interpretations of the median stylus were studied and tested in a phylogenetic context. The median stylus and other phallic homologies were revisited and redefined. All studied genera were found to be monophyletic.
Similar content being viewed by others
References
Aldrich, J.M. (1916). Sarcophaga and allies in North America. La Fayette, Indiana: Entomological Society of America, Thomas Say Foundation.
Amat, E., Ramírez-Mora, M. A., Buenaventura, E., & Gómez-Piñerez, L. M. (2013). Variación temporal de la abundancia en las familias de moscas carroñeras (Diptera, Calyptratae) en un valle andino antropizado de Colombia. Acta Zoologica Mexicana, 29, 463–472.
Amorim, D. S., Silva, V. C., & Balbi, M. I. (2002). Estado do conhecimento dos dípteros neotropicais. In C. Costa, S. A. Vanin, J. M. Lobo, & A. Melic (Eds.), Proyecto de Red Iberoamericana de Biogeografía y Entomología Sistemática PrIBES, Monografias Tercer Milenio (pp. 29–36). Zaragoza: Sociedad Entomológica Aragonesa.
Arnqvist, G., & Danielsson, I. (1999). Copulatory behavior, genital morphology and male fertilization success in water striders. Evolution, 53, 147–156.
Barros, R., Mello-Patiu, C. A., & Pujol-Luz, J. R. (2008). Sarcophagidae (Insecta, Diptera) associados à decomposição de carcaças de Sus scrofa Linnaeus (Suidae) em área de Cerrado do Distrito Federal, Brasil. Revista Brasileira de Entomologia, 52, 606–609.
Bermúdez, S. E., Buenaventura, E., Couri, M., Miranda, R. J., & Herrera, J. M. (2010). Mixed myiasis by Philornis glaucinis (Diptera: Muscidae), Sarcodexia lambens (Diptera: Sarcophagidae) and Lucilia eximia (Diptera: Calliphoridae) over Ramphocelus dimidiatus (Avia: Thraupidae) chicks in Panama. Boletín Sociedad Entomológica Aragonesa, 47, 445–446.
Blackith, R., Blackith, R., & Pape, T. (1997). Taxonomy and systematics of Helicophagella Enderlein, 1928 (Diptera, Sarcophagidae) with the description of a new species and a revised catalogue. Studia Dipterologica, 4, 383–434.
Bremer, K. (1988). The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution, 42, 795–803.
Bremer, K. (1994). Branch support and tree stability. Cladistics, 10, 295–304.
Bruneau, A. (1997). Evolution and homology of bird pollination syndromes in Erythrina (Leguminosae). American Journal of Botany, 84, 54–71.
Buenaventura, E., & Pape, T. (2013). Revision of the New World genus Peckia Robineau-Desvoidy (Diptera: Sarcophagidae). Zootaxa, 3622, 1–87.
Buenaventura, E., Camacho, G., García, A., & Wolff, M. (2009). Sarcophagidae (Diptera) de importancia forense en Colombia: claves taxonómicas, notas sobre su biología y distribución. Revista Colombiana de Entomologia, 35, 189–196.
Carvalho, L. M. L., & Linhares, A. X. (2001). Seasonality of insect succession and pig carcass decomposition in a natural forest area in southeastern Brazil. Journal of Forensic Sciences, 46, 604–608.
Carvalho, L. M. L., Thyssen, P. J., Linhares, A. X., & Palhares, F. A. B. (2000). A checklist of arthropods associated with pig carrion and human corpses in Southeastern Brazil. Memorias Instituto Oswaldo Cruz, 95, 135–138.
Couri, M. S., & Pont, A. C. (2000). Cladistic analysis of Coenosiini (Diptera: Muscidae: Coenosiinae). Systematic Entomology, 25, 373–392.
Courtney, G. W., Pape, T., Skevington, J. H., & Sinclair, B. J. (2009). Biodiversity of Diptera. In R. G. Foottit & P. H. Adler (Eds.), Insect biodiversity science and society (pp. 185–222). Oxford: Wiley–Blackwell.
Dahlem, G. A., & Downes, W. L. (1996). Revision of the genus Boettcheria in America North of Mexico (Diptera: Sarcophagidae). Insecta Mundi, 10, 77–103.
Dallwitz, M. J. (1980). A general system for coding taxonomic descriptions. Taxon, 29, 41–6.
Dodge, H. R. (1966). Some new or little-known Neotropical Sarcophagidae (Diptera), with a review of the genus Oxysarcodexia. Annals of the Entomological Society of America, 59, 674–701.
Eberhard, W. G. (1985). Sexual selection and animal genitalia. Cambridge: Harvard University Press.
Eick, G. N., Jacobs, D. S., & Matthee, C. A. (2005). A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (Chiroptera). Molecular Biology and Evolution, 22, 1869–1886.
Ferraz, M. V. (1992). Comparison of the reproductive behavior between isolated Peckia chrysostoma (Wiedemann, 1830) and Adiscochaeta ingens (Walker, 1849) (Diptera: Sarcophagidae) females reared in laboratory. Memórias do Instituto Oswaldo Cruz, 87, 131–139.
Ferraz, M. V. (1993). Interespecific [sic!] competition between Peckia chrysostoma and Adiscochaeta ingens (Diptera: Sarcophagidae) larvae reared in laboratory. Memórias do Instituto Oswaldo Cruz, 88, 189–194.
Fessl, B., & Tebbich, S. (2002). Philornis downsi—a newly discovered parasite on the Galapagos archipelago - a threat for Darwin Finches? Ibis, 144, 445–451.
Giroux, M., & Wheeler, T. A. (2009). Systematics and phylogeny of the Subgenus Sarcophaga (Neobellieria) (Diptera: Sarcophagidae). Annals of the Entomological Society of America, 102, 567–587.
Giroux, M., Pape, T., & Wheeler, T. A. (2010). Towards a phylogeny of the flesh flies (Diptera: Sarcophagidae): morphology and phylogenetic implications of the acrophallus in the subfamily Sarcophaginae. Zoological Journal of the Linnean Society, 158, 740–778.
Givnish, T. J., & Sytsma, K. J. (1997). Homoplasy in molecular vs. morphological data: The likelihood of correct phylogenetic analysis. In T. J. Givnish & K. J. Sytsma (Eds.), Molecular evolution and adaptive radiation (pp. 55–101). New York: Cambridge University Press.
Goloboff, P. A., Farris, J. S., & Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.
Grant, T. (2002). Testing methods: the evaluation of discovery operations in evolutionary biology. Cladistics, 18, 94–111.
Guo, Y., Cai, J., Chang, Y., Li, X., Liu, Q., Wang, X., Wang, X., Zhong, M., Wen, J., & Wang, J. (2011). Identification of forensically important sarcophagid flies (Diptera: Sarcophagidae) in China, based on COI and 16S rDNA gene sequences. Journal of Forensic Sciences, 56, doi: 10.1111/j.1556-4029.2011.01882.x.
Hedges, S. B., & Maxson, L. R. (1996). Re: molecules and morphology in amniote phylogeny. Molecular Phylogenetics and Evolution, 6, 312–314.
Hoch, H. (2006). Systematics and evolution of Iolania (Hemiptera: Fulgoromorpha: Cixiidae) from Hawaii. Systematic Entomology, 31, 302–320.
Holland, B. R., Spencer, H. G., Worthy, T. H., & Kennedy, M. (2010). Identifying cliques of convergent characters: concerted evolution in the Cormorants and Shags. Systematic Biology, 59, 433–445.
Hosken, D. J., & Stockley, P. (2004). Sexual selection and genital evolution. Trends in Ecology and Evolution, 19, 87–93.
Huelsenbeck, J. P., Ronquist, F., Nielsen, R., & Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.
Jensen, D., Svenson, G. J., Song, H., & Whiting, M. F. (2009). Phylogeny and evolution of male genitalia within the praying mantis genus Tenodera (Mantodea: Mantidae). Invertebrate Systematics, 23, 409–421.
Jirón, L., Vargas, L., & Vargas-Alvarado, E. (1983). Four muscoid flies (Sarcophagidae and Muscidae) associated with human cadavers in Costa Rica. Brenesia, 21, 1–5.
Jordaens, K., Sonet, G., Richet, R., Dupont, E., Braet, Y., & Desmyter, S. (2013). Identification of forensically important Sarcophaga species (Diptera: Sarcophagidae) using the mitochondrial COI gene. International Journal of Legal Medicine, 127, 491–504.
Kuhner, M. K. (2009). Lamarc: Estimating population genetic parameters from molecular data. In P. Lemey, M. Salemi, & A. M. Vandamme (Eds.), The phylogenetic handbook: a practical approach to phylogenetic analysis and hypothesis testing (pp. 592–612). Cambridge: Cambridge University Press.
Kutty, S. N., Pape, T., Wiegmann, B. M., & Meier, R. (2010). Molecular phylogeny of the Calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidea and the position of Mystacinobiidae and McAlpine’s fly. Systematic Entomology, 35, 614–635.
Lanfear, R., Calcott, B., Ho, S. Y. W., & Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
Lopes, H. S. (1941). Sôbre o aparelho genital feminino dos “Sarcophagidae” e sua importância na classificação (Diptera). Revista Brasileira de Biologia, 1, 215–221.
Lopes, H. S. (1943). Contribuição ao conhecimento das larvas dos Sarcophagidae com especial referência ao esqueleto cefálico (Diptera). Memórias do Instituto Oswaldo Cruz, 38, 127–163.
Lopes, H. S. (1958). Considerações sôbre as espécies de Peckia Desvoidy, 1830 e de gêneros affins. Anais da Academia Brasileira de Ciências, 30, 212–243.
Lopes, H. S. (1969). Family Sarcophagidae. In N. Papavero (Ed.), A catalogue of the Diptera of the Americas south of the United States (pp. 1–88). São Paulo: Departamento de Zoologia, Secretaria da Agricultura.
Lopes, H. S. (1975). On Engelimyia, new genus for Sarcophaga cassidifera Engel (Diptera, Sarcophagidae). Revista Brasileira de Biologia, 34, 425–430.
Lopes, H. S. (1983). The importance of the mandible and clypeal arch of the first instar larvae in the classification of the Sarcophagidae (Diptera). Revista Brasileira de Biologia, 26, 293–326.
Lopes, H. S., & Kano, R. (1968). Studies on copulation of some sarcophagid flies (Diptera). Taxonomic importance of some features of male and female genitalia. Revista Brasileira de Biologia, 28, 295–301.
Maddison, W. P., & Maddison, D. R. (2011). Mesquite: a modular system for evolutionary analysis. Version 2.75 http://mesquiteproject.org.
McAlpine, J. F. (1981). Morphology and terminology-adults. In J. F. McAlpine, B. V. Peterson, G. E. Shewell, H. J. Teskey, J. R. Vockeroth, & D. M. Wood (Eds.), Manual of Nearctic Diptera, Volume 1, Monograph 27, Agriculture Canada (pp. 9–63). Ottawa: Canadian Government Publishing Centre.
Meiklejohn, K. A., Wallman, J. F., Pape, T., Cameron, S. L., & Dowton, M. (2013). Utility of COI, CAD and morphological data for resolving relationships within the genus Sarcophaga (sensu lato) (Diptera: Sarcophagidae): a preliminary study. Molecular Phylogenetics and Evolution, 69, 133–141.
Méndez, J., & Pape, T. (2003). Biology and immature stages of Peckia gulo (Fabricius, 1805) (Diptera: Sarcophagidae). Studia Dipterologica, 9, 371–374.
Miller, M., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE) (pp. 1–8), 14 November 2010, New Orleans, LA.
Ming, Z., & Dong, Z. (2013). DNA taxonomy of some Sarcophaga species based on the mitochondrial COI gene fragment. Chinese Journal of Applied Entomology, 50, 71–85.
Moura, M., Carvalho, C. J., & Monteiro-Filho, E. (1997). A preliminary analysis of insects of medico-legal importance in Curitiba, State of Paraná. Memórias do Instituto Oswaldo Cruz, 92, 269–274.
Mulieri, P. R., & Mariluis, J. C. (2011). Description of a new species of Macronychia Rondani (Diptera: Sarcophagidae: Miltogramminae), with a key to the New World species of the genus. Zootaxa, 2832, 51–55.
Mulieri, P. R., & Mello-Patiu, C. A. (2013). Revision of the Neotropical genus Malacophagomyia (Diptera: Sarcophagidae) with description of a new species. Zootaxa, 3736, 368–378.
Mulieri, P. R., Patitucci, L. D., Schnack, J. A., & Mariluis, J. C. (2011). Diversity and seasonal dynamics of an assemblage of sarcophagid Diptera in a gradient of urbanization. Journal of Insect Science, 11, 91.
Nixon, K. C., & Carpenter, J. M. (2012). On homology. Cladistics, 28, 160–169.
Oliveira-da-Silva, A., Ale-Rocha, A., & Rafael, J. A. (2006). Bionomia dos estágios imaturos de duas espécies de Peckia (Diptera, Sarcophagidae) em suíno em decomposição em área de floresta no norte do Brasil. Revista Brasileira de Entomologia, 50, 524–527.
Pape, T. (1987). The Sarcophagidae (Diptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica, 19, 1–203.
Pape, T. (1990). Revisionary notes on American Sarcophaginae (Diptera: Sarcophagidae). Tijdschrift voor Entomologie, 133, 43–74.
Pape, T. (1992). Phylogeny of the Tachinidae family-group. Tijdschrift voor Entomologie, 135, 43–86.
Pape, T. (1994). The world Blaesoxipha Loew, 1861 (Diptera: Sarcophagidae). Entomologica Scandinavica Supplement, 45, 1–247.
Pape, T. (1996). Catalogue of the Sarcophagidae of the world (Insecta: Diptera). Memoirs on Entomology, International 8.
Pape, T. (1998). A new genus of Paramacronychiinae (Diptera: Sarcophagidae), argued from a genus-level cladistic analysis. Systematic Entomology, 23, 187–200.
Pape, T., & Mello-Patiu, C. A. (2006). Revision of Engelimyia Lopes, 1975 (Diptera: Sarcophagidae). Zootaxa, 1245, 21–47.
Pape, T., & Thompson, F.C. (2014). Nomenclator Status Statistics, Systema Dipterorum, Version 1.0 in BioSystematics Database of World Diptera, Version 1.5. Available via http://www.diptera.org/FamilyTables.php.
Piwczyński, M., Szpila, K., & Pape, T. (2014). A large-scale molecular phylogeny of flesh flies (Diptera: Sarcophagidae). Systematic Entomology. doi:10.1111/syen.12086.
Rambaut, A., & Drummond, A.J. (2009). Tracer v1.5. Available via http://beast.bio.ed.ac.uk/Tracer.
Ramírez-Mora, M. A., Buenaventura, E., Gómez-P, L. M., & Amat, E. (2012). Updated checklist and new records of Calyptratae carrion flies (Diptera, Schizophora) from Valle de Aburrá and other localities in Colombia. Entomotropica, 27, 27–35.
Reeves, W. K., Pape, T., & Adler, P. H. (2000). Biological notes on New World Sarcophagidae (Diptera). Studia Dipterologica, 7, 497–500.
Roback, S. S. (1954). The evolution and taxonomy of the Sarcophaginae (Diptera, Sarcophagidae). Urbana: University of Illinois Press.
Robineau-Desvoidy, J.B. (1830). Essai sur les myodaires. Mémoires présentés par divers Savans à l’Académie Royale des Sciences de l’Institut de France (Sciences Mathématiques et Physiques), 2, 1–813.
Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
Salviano, R. J. B., Mello, R. P., Beck, L. C. N. H., & Almeida, J. M. (1996). Aspectos Bionômicos de Squamatoides trivittatus (Diptera, Sarcophagidae) sob Condições de Laboratório. Memórias do Instituto Oswaldo Cruz, 91, 249–254.
Scotland, R. W., Olmstead, R. G., & Bennett, J. R. (2003). Phylogeny reconstruction: the role of morphology. Systematic Biology, 52, 539–548.
Sinclair, B. J. (2000). Morphology and terminology of Diptera male terminalia. In L. Papp & B. Darvas (Eds.), Contributions to a manual of Palaearctic Diptera with special reference to flies of economic importance (General and Applied Dipterology, Vol. 1, pp. 53–74). Budapest: Science Herald.
Singh, B., & Wells, J. D. (2013). Molecular Systematics of the Calliphoridae (Diptera: Oestroidea): evidence from one mitochondrial and three nuclear genes. Journal of Medical Entomology, 50, 15–23.
Song, H., & Bucheli, S. R. (2009). Comparison of phylogenetic signal between male genitalia and non-genitalia characters in insect systematics. Cladistics, 25, 1–13.
Song, Z.-k., Wang, X.-z., & Liang, G.-q. (2008). Molecular evolution and phylogenetic utility of the internal transcribed spacer 2 (ITS2) in Calyptratae. Journal of Molecular Evolution, 67, 448–464.
Springer, M. S., Burk-Herrick, A., Meredith, R., Eizirik, E., Teeling, E., O’Brian, S. J., & Murphy, W. J. (2007). The adequacy of morphology for reconstructing the early history of placental mammals. Systematic Biology, 56, 673–684.
Stamper, T., Dahlem, G. A., Clifford, C., & DeBry, R. W. (2012). Phylogenetic relationships of flesh flies in the subfamily Sarcophaginae based on three mtDNA fragments (Diptera, Sarcophagidae). Systematic Entomology, 38, 35–44.
Sugiyama, E., & Kano, R. (1984). Systematics of the Sarcophaginae of the Oriental region based on the comparative morphology of the male genitalia (Diptera, Sarcophagidae). Japanese Journal of Sanitary Zoology, 35, 343–356.
Tibana, R., & Lopes, H. S. (1985). On Brazilian Sarcophagidae (Diptera) with description of two new genera and four new species. Revista Brasileira de Entomologia, 29, 189–198.
Townsend, C. H. T. (1934). Muscoid notes and descriptions. Revista Brasileira de Entomologia, 4, 110–112.
Vairo, K. P., Mello-Patiu, C. A., & Carvalho, C. J. B. (2011). Pictorial identification key for species of Sarcophagidae (Diptera) of potential forensic importance in southern Brazil. Revista Brasileira de Entomologia, 55, 333–347.
Whitfield, J. B., Mardulyn, P., Austin, A. D., & Dowton, M. (2002). Phylogenetic relationships among microgastrine braconid wasp genera based on data from the 16S, COI and 28S genes and morphology. Systematic Entomology, 27, 337–359.
Whitmore, D., Pape, T., & Cerretti, P. (2013). Phylogeny of Heteronychia: the largest lineage of Sarcophaga (Diptera: Sarcophagidae). Zoological Journal of the Linnean Society, 169, 604–639.
Wiens, J. J., Chippindale, P. T., & Hillis, D. M. (2003). When are phylogenetic analyses misled by convergence? A case study in Texas Cave Salamanders. Systematic Biology, 52, 501–514.
Zehner, R., Amendt, J., Schutt, S., Sauer, J., Krettek, R., & Povolný, D. (2004). Genetic identification of forensically important flesh flies (Diptera: Sarcophagidae). International Journal of Legal Medicine, 118, 245–247.
Zloty, J., Sinclair, B. J., & Pritchard, G. (2005). Discovered in our backyard: a new genus and species of a new family from the Rocky Mountains of North America (Diptera, Tabanomorpha). Systematic Entomology, 30, 248–266.
Acknowledgments
We are grateful to Dr. C. Mello-Patiu, Museu Nacional/Universidade Federal do Rio de Janeiro, Rio de Janeiro; Mr. M. Zumbado, Instituto Nacional de Biodiversidad, Santo Domingo, CR; Dr. C. Medina, Instituto Alexander von Humboldt, Villa de Leyva; Mrs. G. Camacho, Instituto Nacional de Medicina Legal y Ciencias Forenses, Bogotá; Dr. N.E. Woodley, USDA National Museum of Natural History, Washington DC; Dr. M. Wolff, Universidad de Antioquia, Medellín; Dr. K. A. Johanson, Swedish Museum of Natural History, Stockholm, for loan of material. This study was supported by the División de Investigación Sede Bogotá of the Universidad Nacional de Colombia (project no. 201010012649 to E. Buenaventura), the Department of Science Technology and Innovation – COLCIENCIAS in Colombia (Grant 512–2010 to E. Buenaventura), the Smithsonian Institution (predoctoral Fellowship 2013 to E. Buenaventura), and the Danish Natural Science Research Council (grant no. 272–08–0480 to T. Pape). E. Buenaventura is thankful to Mr. D. K.-B. Cheung, Natural History Museum of Denmark, Copenhagen, for assistance with SEM micrography, scientific illustration, and composition of plates and to Drs T. Dikow, Smithsonian Institution, National Museum of Natural History, Washington DC, and N.E. Woodley, USDA National Museum of Natural History, Washington DC, for hosting and support during her Smithsonian fellowship. E. Buenaventura is thankful to Dr. C. Sarmiento, Instituto de Ciencias Naturales, Bogotá, for his invaluable help at discussing characters, phylogenetic methods, and correcting an early draft of this paper. We are thankful to Dr. M. Giroux, Department of Natural Resource Sciences of McGill University, Montreal, for sharing SEM images, and for reading and commenting on a late version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 1.84 mb)
Rights and permissions
About this article
Cite this article
Buenaventura, E., Pape, T. Phylogeny of the Peckia-genus group: evolution of male genitalia in the major necrophagous guild of Neotropical flesh flies (Diptera: Sarcophagidae). Org Divers Evol 15, 301–331 (2015). https://doi.org/10.1007/s13127-015-0203-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13127-015-0203-0