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The Phylogeny and Lygodium Fern Host Associations of Musotiminae Moths, Biological Control (2019), Doi: Doi.Org/10.1016/J.Biocontrol.2019.04.004

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The Phylogeny and Lygodium Fern Host Associations of Musotiminae Moths, Biological Control (2019), Doi: Doi.Org/10.1016/J.Biocontrol.2019.04.004 Accepted Manuscript Scrutinizing biological control survey data from the native range – the phylog- eny and Lygodium fern host associations of Musotiminae moths Graham A. McCulloch, Jeffrey R. Makinson, Ryan Zonneveld, Matthew F. Purcell, Dean R. Brookes, Komal Gurdasani, Ellen C. Lake, S. Raghu, Gimme H. Walter PII: S1049-9644(19)30115-X DOI: https://doi.org/10.1016/j.biocontrol.2019.04.004 Reference: YBCON 3966 To appear in: Biological Control Received Date: 12 February 2019 Revised Date: 11 April 2019 Accepted Date: 12 April 2019 Please cite this article as: McCulloch, G.A., Makinson, J.R., Zonneveld, R., Purcell, M.F., Brookes, D.R., Gurdasani, K., Lake, E.C., Raghu, S., Walter, G.H., Scrutinizing biological control survey data from the native range – the phylogeny and Lygodium fern host associations of Musotiminae moths, Biological Control (2019), doi: https:// doi.org/10.1016/j.biocontrol.2019.04.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Scrutinizing biological control survey data from the native range – the phylogeny and Lygodium fern host associations of Musotiminae moths Graham A. McCulloch1,2*, Jeffrey R. Makinson3, Ryan Zonneveld3, Matthew F. Purcell3, Dean R. Brookes1, Komal Gurdasani1, Ellen C. Lake4, S. Raghu3, Gimme H. Walter1 1 School of Biological Sciences, The University of Queensland, St. Lucia, Queensland, Australia, 4072 2 Department of Zoology, University of Otago, PO Box 56, Dunedin, 9054, New Zealand 3 United States Department of Agriculture, Agricultural Research Service, Australian Biological Control Laboratory, c/o CSIRO, GPO Box 2583, Brisbane, Queensland, Australia, 4001 4 United States Department of Agriculture, Agricultural Research Service, Invasive Plant Research Laboratory, 3225 College Avenue, Fort Lauderdale, FL, 33314, USA *To whom correspondence should be addressed. Email: [email protected] Running title: Lygodium moth systematics Abstract Lygodium microphyllum is considered one of the most damaging environmental weeds in Florida. Despite substantial efforts to control this fern, it continues to spread rapidly through the Greater Everglades ecosystem and other regions of Florida. Biological control is considered a critical component of the management strategy to control this weed, and foreign exploration for natural enemies is ongoing. A number of crambid moths from the subfamily Musotiminae are considered the most promising of the potential biological control agents found to date, because they are relatively abundant on Lygodium and apparently host-specific. We amplified three genes (COI, 18S rRNA and 28S rRNA) to assess the phylogenetic relationships among these moths in relation to geography. Limited genetic structuring was typical within each moth species, and no obvious signals of unrecognised host-specific cryptic species were detected, though further investigation is required, particularly for Eugauria albidentata. Our results emphasize the value of complementing initial field surveys with molecular screening, as such an approach provides valuable information on the biogeographic distribution, genetic structuring, and field host range of potential biological control agents. Keywords Florida, Lygodium microphyllum, Molecular screening, Native range surveys, Old World climbing fern, Crambidae, Systematics 1. Introduction 2 Foreign exploration for natural enemies of an invasive weed is usually an essential initial phase of any successful biological control program (Purcell et al., 2004; Zwölfer et al., 1976). These surveys are typically difficult, both technically and logistically, and can be very time- consuming and expensive (Goolsby et al., 2006). The primary aim of such surveys is to provide a list of herbivores associated with the target weed (Purcell et al., 2004), and thus provide the background for making decisions about the potential of different organisms as biological control agents. However, the surveys from foreign exploration are seldom comprehensive because political, practical and/or financial considerations often intrude (Goolsby et al., 2006). Nevertheless, vital information can be derived from these surveys, especially in terms of providing a framework for testing crucial aspects of the host associations, species status and evolutionary history of the species concerned. Biological control practitioners increasingly incorporate modern molecular techniques to assess the relationships within and among potential biological control agents (see Gaskin et al., 2011). Such genetic screening, however, is seldom employed in the initial stages of foreign exploration for biological control agents. Here we assess the value of incorporating molecular screening at the foreign exploration stage of a biological control project, focusing on one subfamily of the lepidopteran natural enemies of the invasive fern Lygodium microphyllum (Pteridophyta: Lygodiaceae). Lygodium microphyllum, also known as Old World climbing fern, is a damaging invasive environmental weed that was first reported as naturalized in Florida, USA, in 1965 (Beckner, 1968). It has since spread across a broad area of southern and central Florida. Range expansion is ongoing, with establishment as far north as Jacksonville (EDDMapS, 2018; 3 Pemberton, 1998; Rodgers et al., 2014). This fern grows rapidly and indeterminately into a vine with individual fronds capable of reaching 30m in length (Hutchinson et al., 2006; Pemberton and Ferriter, 1998). The twining fronds of L. microphyllum climb over trees and shrubs, forming thick rachis mats that smother or shade understorey vegetation (Nauman and Austin, 1978; Pemberton and Ferriter, 1998). Dense rachis mats on the ground and thick skirts of rachises climbing trees can carry fire into habitats that do not normally burn , and if the canopy burns the tree may die (Hutchinson et al., 2006; Pemberton and Ferriter, 1998). These climbing ferns are particularly damaging in the Greater Everglades ecosystem, where their presence results in the destruction of entire tree islands. Lygodium microphyllum is therefore considered one of the most serious invasive weeds impacting the state (FLEPPC, 2017; Volin et al., 2004). Lygodium microphyllum continues to spread rapidly through Florida (EDDMapS, 2018; Humphreys et al., 2017; Rodgers et al., 2014; Volin et al., 2004), despite substantial control efforts against it (Hutchinson et al., 2006; Hutchinson, 2010; Stocker et al., 2008). Traditional management tools such as herbicide applications, prescribed fire, and mechanical controls can be expensive, damage native plant communities, and may be difficult to apply to remote infestations of L. microphyllum (Hutchinson et al., 2006). Biological control can complement existing management tools, and the integration of weed management techniques may provide more effective control (Hutchinson et al., 2006; Lake and Minteer, 2018; Pemberton and Ferriter, 1998). The native range of L. microphyllum includes tropical and subtropical areas of Asia, Australia, the Pacific Islands and Africa (Pemberton, 1998). The search for natural enemies 4 has focused on the Asian and Australian regions of this range, partially due to early molecular work suggesting that the L. microphyllum present in Florida was more closely related to plants in this region than those in Africa (Goolsby et al., 2003). Also, the diversity of Lygodium species is high in Asia and Australia, increasing the likelihood of the presence of specialist herbivores (Goolsby et al., 2003). Foreign exploration across Australia and Asia has identified a number of arthropod herbivores of Lygodium, including more than 20 insect species (Goolsby et al., 2003). The most prominent herbivores associated with L. microphyllum are crambid moths from the subfamily Musotiminae (Goolsby et al., 2003), being present in well over 1000 collections (made across 21 years) from across the native distribution of the fern. This large crambid subfamily includes 193 described species whose larvae feed entirely on ferns and bryophytes (Nuss et al., 2003; Regier et al., 2012). Nine Musotiminae species (two yet to be described) have been found feeding on L. microphyllum (Table 1). Two additional Musotiminae species, Neomusotima fuscolinealis and Siamusotima aranea, have been found associated exclusively with the congeneric L. japonicum and L. flexuosum respectively (Table 1; Bennett and Pemberton, 2008; Solis et al., 2005). Larvae of these Musotiminae moths are either defoliators of the pinnae (leaflets) or are ‘stem borers’, feeding on the protostele within the rachises and into the rhizome (Solis et al., 2017; Solis et al., 2005; Yen et al., 2004). Two defoliators, N. conspurcatalis and Austromusotima camptozonale, were approved for release by regulatory authorities in Florida following host-range testing, but only N. conspurcatalis established (Boughton and Pemberton, 2008; Boughton and Pemberton, 2009; McCulloch et al., 2018; Smith et al., 2014). Neomusotima conspurcatalis is currently being mass-reared and released in Florida as part of the Comprehensive Everglades Restoration Plan (CERP). An additional 5 Musotiminae defoliator,
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