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The Phylogenetic Conundrum of Lutzia (Diptera: Culicidae: Culicini): a Cautionary Account of Conflict and Support

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The Phylogenetic Conundrum of Lutzia (Diptera: Culicidae: Culicini): a Cautionary Account of Conflict and Support Title The phylogenetic conundrum of Lutzia(Diptera: Culicidae: Culicini): a cautionary account of conflict and support Authors Kitching, I; Culverwell, CL; Harbach, RE Date Submitted 2016-04-12 Insect Systematics & Evolution 46 (2015) 269–290 brill.com/ise The phylogenetic conundrum of Lutzia (Diptera: Culicidae: Culicini): a cautionary account of conflict and support Ian J. Kitching, C. Lorna Culverwell and Ralph E. Harbach* Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK *Corresponding author, e-mail: [email protected] Published online 12 May 2014; published online 10 June 2015 Abstract Lutzia Theobald was reduced to a subgenus ofCulex in 1932 and was treated as such until it was restored to its original generic status in 2003, based mainly on modifications of the larvae for predation. Previous phylogenetic studies based on morphological and molecular data have provided conflicting support for the generic status of Lutzia: analyses of morphological data support the generic status whereas analyses based on DNA sequences do not. Our previous phylogenetic analyses of Culicini (based on 169 morpho- logical characters and 86 species representing the four genera and 26 subgenera of Culicini, most informal group taxa of subgenus Culex and five outgroup species from other tribes) seemed to indicate a conflict between adult and larval morphological data. Hence, we conducted a series of comparative and data exclu- sion analyses to determine whether the alternative positions of Lutzia are due to conflicting signal or to a lack of strong signal. We found that separate and combined analyses of adult and larval data support dif- ferent patterns of relationships between Lutzia and other Culicini. However, the majority of conflicting clades are poorly supported and once these are removed from consideration, most of the topological dis- parity disappears, along with much of the resolution, suggesting that morphology alone does not have sufficiently strong signal to resolve the position ofLutzia . We critically examine the results of other phy- logenetic studies of culicinine relationships and conclude that no morphological or molecular data set analysed in any study conducted to date has adequate signal to place Lutzia unequivocally with regard to other taxa in Culicini. Phylogenetic relationships observed thus far suggest that Lutzia is placed within Culex but further data and extended taxon sampling are required to confirm its position relative to Culex. Keywords Culicomorpha; morphology; phylogeny; systematics; taxonomy Introduction Culicini (Diptera: Culicidae: Culicinae), the second largest tribe of mosquitoes, includes 795 currently recognised species classified into four genera:Culex Linnaeus, the largest, has 768 species, Deinocerites Theobald has 18 species, Galindomyia Stone & Barreto one species and Lutzia Theobald has eight species. Lutzia was established by © 2015 Natural History Museum DOI 10.1163/1876312X-45032119 This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercialDownloaded from Brill.com03/31/2020 3.0 Unported 09:41:32AM (CC BY-NC 3.0) License, http://creativecommons.org/licenses/by-nc/3.0/ via free access 270 I.J. Kitching et al. / Insect Systematics & Evolution 46 (2015) 269–290 Theobald (1903) as a distinct genus for the Neotropical species Culex bigoti Bellardi. Edwards (1932) reduced Lutzia to a subgenus of Culex and subsequent authors accepted this subgeneric status. Belkin (1962a) surmised that “Lutzia is a very ancient derivative” of Culex, with apparently strongest affinities with subgenusCulex . Although Tanaka et al. (1979) treated Lutzia as a subgenus, they felt it was “more rea- sonable to consider Lutzia as a genus” because it was morphologically more distinct than other subgenera of Culex. Acting on this suggestion, Tanaka (2003) formally restored Lutzia to its original generic status. Species of Lutzia occur in the Afrotropical, Oriental, southern Palaearctic, Australasian and Neotropical regions. The adults are large mosquitoes, larger than spe- cies of genus Culex. The larvae are predaceous, principally on larvae of other mosquito species. The immature stages predominantly inhabit ground-water habitats, but are occasionally found in phytotelm and artificial containers. Females attack domestic ani- mals and sometimes humans, but otherwise very little is known of the bionomics of the adults. Genus Lutzia is based mainly on the modifications of the larvae for predation; few characters of the adults are regarded as sufficiently distinctive to justify the separation of the group from genus Culex. The maxillary palpi of males are longer than the pro- boscis with the distal two palpomeres upturned and setose (except in Lt. shinonagai (Tanaka, Mizusawa & Saugstad) of subgenus Insulalutzia); the palpi of females are no more than one quarter the length of the proboscis. The lower mesepimeral setae are long and four to eight in number (usually one, but infrequently 2–4 and rarely 5, are present in Culex; CLC & REH, unpublished data). The anterior surfaces of the femora and tibiae of the fore- and midlegs are mottled with patches of pale scales. The gono- coxite of the male genitalia lacks scales, the subapical lobe bears three prominent setae (setae a–c) but lacks a foliform seta (seta g), and the phallosome is simple, formed of a single pair of lateral sclerites (as in species of subgenus Culex, lateral and aedeagal scle- rites are not distinguished). The mouthparts of the larvae are highly modified for pre- dation. The lateral palatal brushes consist of about 40 stout and strongly pectinate elements and the mandibles have large teeth for capturing and holding prey. The siphon is short with a continuous mid-posterior row of setae, and the pecten usually extends the whole length of the siphon (except in Lt. shinonagai where is it confined to mid-length). The sclerotized dorsal surface of the terminal segment (segment X) is strongly extended caudad, making the segment appear long and pointed. A number of published and unpublished phylogenetic studies based on morphologi- cal and molecular data support the monophyly of all of the generic-level groups of Culicini except subgenera Culex, Eumelanomyia Theobald and Neoculex Dyar (Mallampalli 1995; Miller et al. 1996; Isoe 2000; Navarro & Liria 2000; Juthayothin 2004; St John 2007; Deus 2009; Vesgueiro et al. 2011; Demari-Silva et al. 2011; Harbach et al. 2012). However, despite this agreement, and bearing in mind the gener- ally limited number of taxa and restricted morphological and molecular data analysed in some of these studies, as well as the use of different methods of phylogenetic and phenetic analysis, the results provide conflicting support for the generic status ofLutzia . With the exception of Mallampalli (1995), analyses based solely on morphological data Downloaded from Brill.com03/31/2020 09:41:32AM via free access I.J. Kitching et al. / Insect Systematics & Evolution 46 (2015) 269–290 271 support the generic status of Lutzia (Navarro et al. 2000; St John 2007; Harbach et al. 2012) by placing it outside the clade comprised of the subgenera of Culex (and also genera Deinocerites and Galindomyia, in studies where these were included). In stark contrast, analyses based on DNA sequence data (ITS1 and ITS2 rDNA and COI mtDNA) do not, placing Lutzia instead among species or subgenera of genus Culex (Miller et al. 1996; Deus 2009; Vesgueiro et al. 2011; Demari-Silva et al. 2011). Our preliminary studies in connection with a broader study of culicinine relation- ships suggested that there is also conflict between adult and larval morphological data when analysed separately and in combination; thus, the present comparative study was undertaken to investigate in more detail whether the alternative positions of Lutzia are genuinely due to signal conflict or simply a lack of strong signal. Materials and methods Morphology We added six species to the data set of 86 species analysed by Harbach et al. (2012): Culex (Culex) annulirostris Skuse, Cx. (Cux.) quinquefasciatus Say, Cx. (Culiciomyia) semibrunneus Edwards, Cx. (Eumelanomyia) insignis (Carter), Cx. (Lophoceraomyia) mammilifer (Leicester) and Cx. (Lop.) rubithoracis (Leicester) (see Harbach et al. 2012 for authorship of the other species mentioned herein, and all species included in the analyses). These species were added because the data were already available from another study and on the premise that they would strengthen support for the groups to which they belong. The full data set of 92 taxa thus comprised an ingroup of 87 species of Culicini and five outgroup species from other tribes of subfamily Culicinae: Culiseta (Culiseta) annulata (Culisetini), Mansonia (Mansonia) titillans (Mansoniini), Maorigoeldia argyropus (Sabethini), Orthopodomyia anopheloides (Orthopodomyiini) and Psorophora (Psorophora) ciliata (Aedini). The ingroup includes the type species of most generic-level taxa and the nominotypical species of all informal species groups and subgroups of subgenus Culex (Harbach 2011), except for the Coronator and Guiarti Groups. The 169 anatomical characters used by Harbach et al. (2012), fourth- instar larvae (76), pupae (15), adults (47), male genitalia (30) and habitat of immature stages (1), were coded for the six added species, using the protocols described in that paper, and these data are presented in Table 1. Missing data are indicated by “?”, and characters that could not be scored due to absence
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