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Diptera: Tachinidae), Based on Morphological Characters

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Diptera: Tachinidae), Based on Morphological Characters Rodrigo de Vilhena Perez Dios Cladistic analysis of Phasiinae (Diptera: Tachinidae), based on morphological characters. Análise cladística de Phasiinae (Diptera: Tachinidae), baseada em caracteres morfológicos São Paulo 2019 Rodrigo de Vilhena Perez Dios Cladistic analysis of Phasiinae (Diptera: Tachinidae), based on morphological characters. Análise cladística de Phasiinae (Diptera: Tachinidae), baseada em caracteres morfológicos Tese apresentada ao Instituto de Biociências da Universidade de São Paulo, para a obtenção de Título de Doutor em Ciências Biológicas, na Área de Zoologia. Orientador(a): Prof. Dr. Silvio Shigueo Nihei São Paulo 2019 General abstract Among the highly diverse class Insecta, the order Diptera, comprising flies and mosquitoes, is one of the most diverse. The order also presents an enormous diversity of life habits and morphology variation in all its life stages. Tachinidae, one of the Diptera families with the highest number of species, are known for its parasitoid habits of other Arthropoda. Phasiinae, a Tachinidae subfamily, is historically known for being parasitoid of heteropteran bugs and therefore its importance for biological control, as many of its hosts are agricultural pests. Phasiinae is currently classified into 103 genera with ca 620 species worldwide. Despite being the smaller Tachinidae subfamily, they present a wide range of morphological variation, mainly in the terminalia. The subfamily systematics was studied recently with molecular data, but some questions remain regarding its internal relationships. We propose a phylogenetic analysis of Phasiinae using 183 morphological characters, sampling 72 genera from all tribes and all zoogeographical regions. Phasiinae is corroborated as monophyletic, as well as most of its tribes; some taxonomic changes were made and the subfamily classification updated following the phylogenetic hypothesis. The basal relationships of Phasiinae and between some tribes still have uncertainties, and further studies are required. During the morphological study we were able to explore more deeply the less known female terminalia of Phasiinae. A diagnosis for the female terminalia of each Phasiinae tribe is presented, as well as some new homologies proposed and discussed. Combining both chapters, we have also further explored the evolution of the two main oviposition strategies in the subfamily and their associated morphology: the strategy of piercing the host and the strategy of laying large planoconvex eggs externally on the host. Both apparently evolved more than once in Phasiinae. The present study can contribute to new systematic studies, as well as further allowing host-parasite evolutionary studies. Keywords: Systematics, morphology, terminalia, parasitoids Resumo geral Entre a extremamente diversa classe Insecta, a ordem Diptera, a qual fazem parte as moscas e os mosquitos, é uma das mais diversas. A ordem apresenta uma enorme diversidade de hábitos de vida e de variação morfológica em todas os seus estágios de vida. Tachinidae, uma das famílias de Diptera, está entre as mais numerosas em números de espécies, sendo conhecida por ser parasitoide de outros Arthropoda. Phasiinae, uma das famílias de Tachinidae, é historicamente conhecida por serem parasitoides de insetos da ordem Heteroptera, e, portanto, possuindo importância para o controle biológico, já que alguns dos seus hospedeiros são pestes agrícolas. Phasiinae está classificada atualmente em 2013 gêneros, com cerca de 620 espécies distribuídas por todo o planeta. Apesar de ser a menor subfamília de Tachinidae, apresentam uma grande diversidade morfológica, principalmente em suas terminalias. Recentemente a subfamília foi abordada em um estudo sistemático com dados moleculares, porém ainda existem questões relacionadas aos seus relacionamentos internos. Estamos propondo uma nova análise filogenética de Phasiinae, usando 183 caracteres morfológicos e amostrando 72 gêneros de todas as suas tribos e de todas as regiões zoogeográficas. A subfamília Phasiinae é corroborada como monofilético, assim como a grande maioria de suas tribos; propomos algumas mudanças taxonômicas e a classificação da subfamília é atualizada baseado no resultado filogenético. As relações basais de Phasiinae e o relacionamento interno entre algumas tribos ainda estão incertos, e mais estudos são necessários. Ao longo do estudo morfológico, pudemos explorar mais afundo as características da menos conhecida genitália feminina de Phasiinae. Com isso, apresentamos uma diagnose usando a terminalia feminina para todas as suas tribos, assim como propomos algumas novas homologias e as discutindo. Combinando os dois capítulos, exploramos a evolução das estratégias de oviposição na subfamília e sua morfologia associada: a estratégia de perfurar o hospedeiro, e a estratégia de colocar grandes ovos plano-convexos externamente ao hospedeiro. As duas aparentemente evoluíram mais de uma vez em Phasiinae. O presente estudo poderá contribuir para novos estudos de sistemática filogenética, assim como possibilitar estudos futuros com evolução da associação parasita hospedeiro. Palavras-chave: Sistemática, morfologia, terminalia, parasitoides. General introduction Tachinidae flies are parasitoids of a wide range of arthropods. There are records of tachinids parasitizing 15 orders of arthropods, including many orders of insects, and more rarely chilopods and scorpions (Arnaud, 1978; Stireman et al., 2006). Excluding Hymenoptera, Tachinidae represent the largest group of insect parasitoids (Eggleton & Belshaw, 1992). The family is also one of the most diverse within Diptera, with ~8500 species worldwide and at least the same number of undescribed species from a conservative estimate (O’Hara, 2013, O’Hara et al., 2019). Nowadays, the Neotropical fauna is the most diverse, with 3032 described species (Guimarães, 1971, O’Hara et al., 2019). Despite their diversity, recent studies with molecular data present the family as a relatively recent group, tracing its origin to 30-40 million years ago (Wiegmann et al., 2011, Cerretti et al., 2017). Tachinids are very important to natural regulators of herbivorous populations, and also structure ecological communities. They are widely used as biological control, with over 100 species used as pest control agents in different countries (Grenier, 1988; Stireman et al., 2006). Despite their importance, there is a lack of knowledge regarding the family, and its species are poorly known in different aspects regarding taxonomy, systematics, morphology, hosts and biology (Stireman et al., 2019). Tachinidae organization and composition have been changing for a long time (O’Hara, 2013). Nowadays four subfamilies are usually recognized in Tachinidae: Dexiinae, Exoristinae, Phasiinae and Tachininae (Cerreti et al., 2014, O’Hara et al., 2019, Stireman et al., 2019). Tachinidae species are highly diverse morphologically, with many striking features and convergent characteristics between its internal groups, which is one of the obstacles for its classification (Tschorsnig, 1985, Stireman et al., 2006, O’Hara, 2013, Cerretti et al., 2014). Tachinidae females present different reproduction strategies that have helped researchers classify tachinids before using phylogenies (Stireman et al., 2006, O’Hara, 2013). We can classify these strategies into some common groups. Some tachinids lay large plano- convex eggs (sometimes called macrotype eggs) directly on hosts (which can be embryonated or not). A second kind of strategy involves piercing the host to inject eggs or larvae. Other tachinids deposit a pharate larvae on the host or close to it (the larvae actively search for the host). Another group has females that lay miniscule eggs (called “microtype” eggs) on leaves, which are ingested by the host and hatch inside its digestive system. Nowadays we know that most of these strategies have probably developed more than once in different Tachinidae groups and are not homologous. For example, piercers originating from different tergites or macrotype eggs with different external structures. Despite that, there are many questions that still need to be investigated regarding Tachinidae reproductive strategies (Cerreti et al., 2014 Blaschke et al., 2018, Stireman et al., 2019). Morphological studies including terminalia, as well as other reproductive traits (as oviposition and eggs), immature stages and puparia were essential for the stabilization of the taxonomic organization of Tachinidae (Herting, 1957, Dupuis, 1963, Verbeke, 1963, Tschorsnig, 1985, Cantrell, 1988, Ziegler, 1998, O’Hara, 2013). The first studies with a phylogenetic framework were also enlightening for Tachinidae. The corroboration of their monophyly, as well as some internal clades, were usually obtained; but many questions still remained to be investigated and new ones emerged (Pape, 1992, Stireman, 2002, Tachi & Shima, 2010). Despite that, no extensive systematic study has been carried out focusing on the whole family and with a large sampling until the last decade. New research has been addressing Tachinidae as a whole or focusing on one subfamily, using morphology and/or molecular data (Cerretti et al., 2014, Winkler et al., 2015, Blaschke et al., 2018, Stireman et al., 2019). Some results seem to be convergent, while others still need to be addressed. The subfamilies are not all considered monophyletic in all publications (Phasiinae and Exotistinae are commonly found as monophyletic), and three new subfamilies could be proposed (Macquartiini + Myophasiini and
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