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Life on the Fly: Ecology and Evolution of the Helicopter Damselflies

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Life on the Fly: Ecology and Evolution of the Helicopter Damselflies Life on the Fly: Ecology and Evolution of the Helicopter Damselflies (Odonata: Pseudostigmatidae) Spencer J. Ingley [email protected] (352) 278-2705 Department of Wildlife Ecology and Conservation Advisor: Dr. Marc Branham CALS Honors Program ABSTRACT Helicopter damselflies (Pseudostigmatidae: Odonata) form a relatively small, yet dynamic group of endangered odonates (including the largest extant odonate, Megaloprepus caerulatus, with a wingspan of ~190 mm). This highly specialized group is found in primary- growth rainforest (Central and South America; one East African species) where they oviposit exclusively in phytotelmata and are specialist foragers on orb weaver spiders which are plucked from their web. Pseudostigmatids exhibit unique wing structure within Zygoptera, and within Pseudostigmatidae both broad and narrow wing forms exist. Oviposition, spider feeding, and wing form evolution are examined for the first time within an evolutionary context using modern phylogenetic methods of tree reconstruction and character optimization. Phylogenetic analyses (Bayesian and Parsimony) were performed on a data set composed of 60 morphological characters and ~3.4kb of sequence data (Mitochondrial loci: 12S, 16S, COII; Nuclear loci: 28S, H3). Findings include monophyletic Pseudostigmatidae, Coryphagrion grandis (East African species) as the sister group to all Neotropical genera, and Pericnemis as sister to Pseudostigmatidae. The genera Mecistogaster and Pseudostigma are monophyletic while Microstigma forms a monophyletic group with Megaloprepus. Oviposition in phytotelmata likely evolved multiple times within Zygoptera, and spider feeding evolved from a single origin. There are two separate origins of narrow wings within Pseudostigmatidae. These findings provide new insight into Pseudostigmatid evolution that can be used to generate awareness of the threatened status of Helicopter damselflies. KEY WORDS Helicopter Damselflies, Odonata, Behavioral evolution, wing morphology, oviposition, spider feeding. INTRODUCTION Odonata, the insect order that is comprised of Damselflies (Zygoptera) and Dragonflies (Epiprocta), is one of the most ancient winged insect groups (~300 MYA). Odonata is comprised of roughly 5,500 species, and has a worldwide distribution. Odonates are among the most acrobatic flyers in the world. Using four wings capable of moving independently, they are equally adept at snatching either a mate or prey out of the air. Of the known species, over 600 are listed on the International Union for Conservation of Nature (IUCN) Red List for endangered and threatened species (IUCN Red List Website, http://www.iucnredlist.org/search). For these and other reasons, odonates are gaining momentum as an organism important to conservation efforts worldwide (Polhemus, 1997; Samways and Steytler, 1996; Painter, 1999; Hawking and New, 1999). Perhaps the biggest impediment to their success as a conservation tool is the lack of knowledge regarding the classification and evolution of taxa below the family level. For effective conservation of biodiversity Ingley 2009 to take place, it is essential that species are Fig.1. (a) Megaloprepus caerulatus: the largest extant Odonate species, which belongs to the family properly identified and classified. Among Pseudostigmatidae; (b) Teinobasis aerial: a „typical‟ damselfly in terms of size and morphology. the most spectacular of all odonates are the Helicopter damselflies (Zygoptera: Pseudostigmatidae; Figure 1a.). This group is composed of 6 genera and 19 species. Nearly all species of pseudostigmatids inhabit Neotropical rainforests, with one species endemic to east Africa (Coryphagrion grandis). The group is famous for its gigantism and includes the largest extant odonate, Megaloprepus caerulatus, with a wingspan of over 190mm (Groeneveld et al., 2007; Figure 1a.). The evolution of damselfly gigantism has been examined phylogenetically and it is hypothesized to have a single origin attributed only to Helicopter damselflies (Groeneveld et al., 2007). Oviposition Behavior In addition to their extreme size, pseudostigmatids exhibit unique oviposition and feeding behaviors. While most odonates oviposit endophytically in lake and stream vegetation, pseudostigmatids oviposit exclusively in phytotelmata (rain filled, naturally occurring water containers including tree-holes, bamboo, tank bromeliads, and fruit husks; Figure 2) (Corbet, 2004). Though female pseudostigmatids typically land inside or along the margins of Collins 2009 Fig. 2. Megaloprepus caerulatus ovipositing in a tree hole in Costa Rica. This species, along with other members of Pseudostigmatidae, exhibit this behavior of phytotelmata oviposition. Other oviposition habitats include tank bromeliad plants, bamboo internodes, and fruit husks. phytotelmata and deposit their eggs in the water collected within the container, some species have been observed “launching” their eggs into phytotelmata while hovering above (Machado and Martinez, 1982). These behaviors, as well as their unique larval habitat, have been studied extensively for a small number of species (Fincke, 2005; Machado and Martinez, 1982) and documented for nearly all (Fincke, 2005; Corbet, 2004), but have never been examined in an evolutionary context using modern phylogenetic methods. Feeding Behavior While adult odonates typically feed on small flying insects captured while in flight, pseudostigmatids (the only unequivocal specialist foragers within Odonata; Corbet, 2004) Collins 2009 Fig. 3. Mecistogaster ornata approaching an orb-weaver spider web. This species, along with other Pseudostigmatid species, are the only known unequivocal specialist foragers within Odonata, feeding exclusively on orb-weaver spiders plucked from their web. specialize on orb-weaver spiders, which they pluck directly from their webs (Figure 3). Pseudostigmatids have been observed plucking insects caught in webs as well (Corbet, 2004). In addition, pseudostigmatids are known to defend a set of webs within an established territory, a behavior that resembles a sort of harvest tactic, as orb-weaver spiders will use a vacant web instead of spinning a new one (Corbet, 2004). The behavior of web feeding, both on spiders and Collins 2009 their prey caught in the webs, have yet to be examined using modern phylogenetic methods. Wing Form In most zygopterans, including Pseudostigmatidae, a narrow petiolate wing form is common (Figure 4a). However, four pseudostigmatid genera (Anomisma, Microstigma, Megaloprepus, and Pseudostigma) each exhibit an expanded or broadened wing beyond the basal petiolation (Figure 4b). This broadening of the wing is specifically defined as having expansions of intercalated veins and/or dichotomous branching of radial veins from the RP2 vein forward through the CuA vein (Figure 4a, 4b). The extent of the expansion varies among genera. Other groups within Zygoptera exhibit similar wing expansions (i.e. Calopterygiodea) but the origins and directionality (as well as the functional role) of this trait have never been examined. Due to their high level of behavioral and wing structure specialization and their importance to conservation (4 of 19 species of pseudostigmatids are thought to be threatened or endangered; IUCN Red List Website, http://www.iucnredlist.org/search) study of the group is especially urgent. Here, we present the first comprehensive analysis of pseudostigmatid phylogeny, and use this phylogeny to examine the origins and evolution of these unique behavioral and morphological adaptations. Ingley 2009 a. Ingley 2009 b. Fig. 5. Wing forms present in Pseudostigmatidae, showing characterization of the expanded wing form. This expansion or broadening of the wing is herein defined as having expansions of intercalated veins and/or dichotomous branching of radial veins from the RP2 vein forward through the CuA vein. (a) Narrow wing of Mecistogaster lucretia, lacking major innovation of pterostigma and wing expansion. (b) Broad wing for of Microstigma anomalum, showing modified pterostigma and expanded wing form. MATERIALS AND METHODS Taxon sampling Of the 19 recognized species that comprise Pseudostigmatidae, 16 were used in this analysis (Appendix I). Several species in the family, largely due to their conservation status or difficulty in attaining permits in the country of origin (e.g., Brazil), were not available to generate either morphological or molecular data. However, the 16 species included herein represent all six currently recognized pseudostigmatid genera, both from the Old World and New World. Multiple exemplars were obtained and used for morphological character coding (except for Coryphagrion grandis, which I coded from the literature and photographs taken by Seth Bybee of specimens in the collection of The Natural History Museum, London). Outgroups were selected from ten closely related genera, resulting in 14 outgroup taxa (Appendix I). The outgroup sampling was focused on including other coenagrionoid zygopteran taxa that inhabit similar niches (e.g., living in the forest understory) and those exhibiting similar behaviors as pseudostigmatids (i.e., use of phytotelmata as larval habitat). Outgroup taxa represented species from Southeast Asia, the South Pacific, the Caribbean and North, Central, and South America. Lestes disjunctus served as the root taxon for all analyses due to knowledge gained from prior analyses, which provide significant evidence supporting Lestidae as sister to all other zygopterans (Bybee et al., 2008; Carle et al., 2008). This
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