Rodrigo de Vilhena Perez Dios

Cladistic analysis of (Diptera: ), 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 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 , 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 . There are records of tachinids parasitizing 15 orders of arthropods, including many orders of , and more rarely chilopods and scorpions (Arnaud, 1978; Stireman et al., 2006). Excluding Hymenoptera, Tachinidae represent the largest group of 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 , 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: , Exoristinae, Phasiinae and (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 Palpostomatini + Imitomyiini; Stireman et al., 2018; and Dufouriini + Oestrophasiini + Freraeini; Santis & Nihei, in prep.). Phasiinae is the smallest of the four subfamilies, with approximately 620 species in 103 genera (Guimarães, 1971, Crosskey, 1976, Cantrell, 1988, Herting & Dely-Draskovitz, 1993, O’Hara et al., 2009, O’Hara & Cerretti, 2016, Blaschke et al., 2018, Stireman et al., 2019); 55 of those genera are monotypic, a common problem within the Tachinidae family (O’Hara, 2013). The subfamily is historically known for being parasitoids of different families of true bugs (Hemiptera: Heteroptera). The only exception is the tribe Strongygastrini, which has records of Hymenoptera and Coleoptera as hosts, as well as records of Heteroptera. Some Phasiinae flies parasite species that are important agriculture pests, which makes them relevant for biological control studies (Guimarães, 1977, Arnaud, 1978, Dupuis, 1963, Blaschke et al., 2018). Phasiinae species are known to use specialized antennal receptors sensitive to host pheromones as guides to their potential hosts (Aldrich, 1995, Aldrich et al., 2006) Phasiinae species have been historically grouped as usually less bristled flies (compared to standard tachinids). This is just a convergence, as some phasiines are strongly bristled and externally resemble other groups of Tachinidae (e.g. Zitini), and other groups of Tachinidae also have reduced bristles (e.g. ). The subfamily has a wide range of morphological variation, from minute to large species, possibly being the most extreme within Tachinidae (Figure 1). They are also known for possible mimicry with different Hymenoptera, some of which is really remarkable (Blaschke et al., 2018), even though no studies have yet focused on such mimicry. The group has a wide range of oviposition strategies, and different structures that enable them to surpass host barriers. All phasiines are oviparous (all eggs not embryonated), with the ovolarviparous Strongygastrini being the only known exception. Some groups have piercer-like structures that penetrate hosts to inject membranous eggs. These piercers can be derived from different structures, sometimes the eighth sternite (e.g. , Xystini, Catharosiini) or eleventh sternite (). There are also groups that lay large plano-convex eggs, which are attached externally to the hosts (Gymnosomatini). Other groups () developed pincer-like structures from the sixth tergite, besides having an eighth sternite piercer-like (Herting, 1957, Dupuis, 1963, Blaschke et al., 2018). Adults of phasiines usually parasite adults or last-instar nymphs, which are well sclerotized externally (different from the usual Holometabola larvae, hosts for the majority of other tachinids). Accordingly, some researchers have hypothesized that the great variability in the female terminalia and oviposition strategies observed in the group have evolved in response to their hosts’ hard exoskeleton, and the males could have also “responded” to those adaptations (Rubtzov, 1951, Verbeke, 1962 Dupuis, 1963, Blaschke et al., 2018). In the earlier literature, Phasiinae was presumed to be a basal Tachinidae lineage, as their oviparous condition was primitive (Mesnil, 1939, Wood 1987, Richter, 1992, Stireman et al., 2006). Others disagree, and consider Phasiinae as a derived clade, mentioning characteristics such as the complicated terminalia and the setae which probably reduced (Emden, 1945, Herting, 1983). Its relationship within Tachinidae has also been debated, sometimes being grouped with Exoristinae based on their oviposition and egg types (Herting, 1966, Mesnil, 1966) or with Dexiinae (Shima, 1989). In the recent phylogenetic studies, Phasiinae is always a derived lineage, being a sister group to a paraphyletic or monophyletic Dexiinae (Cerretti et al., 2014, Blaschke et al., 2018, Stireman et al., 2019; Santis & Nihei, in prep.). Phasiinae and Exoristinae are the only Tachinidae subfamilies whose systematics were studied individually based on molecular data (Stireman, 2002; Blaschke et al., 2018), the latter less extensively using only two genes and lower sampling. In that publication, the subfamily was considered monophyletic and many groups with doubtful placement were resolved (e.g. Epigrimyiini, Eutherini, Parerigonini, Strongygastrini and the Litophasia Girshcner, 1887). One putative morphological synapomorphy was mentioned: “an elongated medial plate of the hypandrium in males”. Stireman et al. (2019), focused on the whole family, and other than a few nots, little was discussed about Phasiinae as the authors mentioned that their data derived from the previous published work (Blaschke et al., 2018). The second publication had a few discrepancies from the previous work, as it had a broader sample and aim, as well as a few more Phasiinae taxa. The morphology and notability of Phasiinae always greatly impacted researchers, as they were fascinated by their wide variety of forms, as well as the striking terminalia features (both male and female), being considered by many as one of the most diverse in Diptera (Rubtzov, 1951, Herting, 1957, Verbeke, 1962, Dupuis, 1963, Verbeke, 1963, Tschorsnig 1985, Blaschke et al., 2018). The connection with their hosts has probably been essential for the development of this wide range of structures, especially for females, as a way to overcome the barriers of hard-sclerotized hosts (Rubtzov, 1951, Dupuis, 1963, Blaschke et al., 2018). Even with all the recent efforts, there is no consensus about many questions regarding Phasiinae systematics. Considering the potential importance of the group for biological control, and the connection of their morphology with their hosts, more studies in both areas are needed. This study focuses on some of these questions and brings new knowledge to these areas. We propose (mostly new) morphological synapomorphies for the subfamily and tribes, as well as corroborate their monophyly. With a detailed study of the male and female terminalia, new homologies can be proposed, and their structures can be well understood. Both parts can help get a better understanding of the relationships within the subfamily, as well as the host/parasitoid connection. Furthermore, all the new data can be used for different areas, including biological control of important pests.

General conclusions

The wide morphological study of the subfamily Phasiinae presented here, gives new information regarding the subfamily systematic relationships, as well as their morphological characteristics, with great emphasis on male and female terminalia. In the presented systematic analysis, the subfamily Phasiinae is recovered monophyletic as in previous studies. Most of the tribes are recovered as monophyletic: Catharosiini, Cylindromyiini, Gymnosomatini, Hermyini, Leucostomatini, Parerigonini, Phasiini, Strongygastrini, Xystiini, Zitini. The tribes Tarassini and Euscopoliopteryigini are synonymized with Gymnosomatini. In the tribe Zitini, the genera Australotachina and Pygidimyia are in great need of taxonomic revision, which could elucidate and change their systematic position and relationship. We have also made a few taxonomic changes, and a few genera changed tribes. Some Phasiinae and Tachinidae taxa still remains in doubtful positions, and more studies are needed. Even though the monophyly of the tribes is well corroborated, their relationships still need further studies, which could be done combining molecular and morphological data, and maybe adding some more taxa. A succinct comparative diagnosis of the less studied female terminalia for each Phasiinae tribe is also provided. Some new homologies for a few structures in some tribes were proposed. We have made some comments on the general morphology of Phasiinae female terminalia, but we intend to expand and improve that discussion in the future, as well as elaborate an identification key for the Phasiinae tribes using the female terminalia. Our study also brings new evidence for the evolution of different oviposition strategies. Two main strategies are recognized for Phasiinae: one using piercer structures to inject membranous eggs; and another consisting of attaching large planoconvex eggs on the host. Both are discussed in a phylogenetically and morphological point view. During this project, the first author went to an internship to the USNM and visitid to the CNC. Both institutions collections were a great contribution for the knowledge presented in the thesis. We were able to photograph 79 type species of Phasiinae, as well as males and females of other 65 species of Phasiinae (the type photos will be available at the USNM website). A total of 88 terminalias were illustrated during the visits. All this data will be really useful in future taxonomic and systematic studies of Phasiinae (some taxonomic works already in progress). All the knowledge and data presented and generated here can be really helpful for future studies. With a stronger phylogenetic framework, as well as evolutionary hypotheses related to their morphology, this thesis can also contribute greatly to future studies related to taxonomy and systematics, as well as host association and coevolution studies and ultimately might be useful for research on using Phasiinae species for biological control.

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