Hymenoptera: Vespidae: Vespinae)
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Cladistics Cladistics (2015) 1–20 10.1111/cla.12138 Phylogeny, landmark analysis and the use of wing venation to study the evolution of social wasps (Hymenoptera: Vespidae: Vespinae) Adrien Perrarda,*, Federico Lopez-Osoriob and James M. Carpentera aDivision of Invertebrate Zoology, American Museum of Natural History, New York, NY 10024, USA; bDepartment of Biology, University of Vermont, Room 120A Marsh Life Science Building, 109 Carrigan Drive, Burlington, VT 05405, USA Accepted 31 July 2015 Abstract Wing venation provides useful characters with which to classify extant and fossil insects. Recently, quantification of its shape using landmarks has increased the potential of wing venation to distinguish taxa. However, the use of wing landmarks in phylo- genetic analyses remains largely unexplored. Here, we tested landmark analysis under parsimony (LAUP) to include wing shape data in a phylogenetic analysis of hornets and yellow jackets. Using 68 morphological characters, nine genes and wing land- marks, we produced the first total-evidence phylogeny of Vespinae. We also tested the influence of LAUP parameters using sim- ulated landmarks. Our data confirmed that optimization parameters, alignment method, landmark number and, under low optimization parameters, the initial orientation of aligned shapes can influence LAUP results. Furthermore, single landmark configurations never accurately reflected the topology used for data simulation, but results were significantly close when com- pared to random topologies. Thus, wing landmark configurations were unreliable phylogenetic characters when treated indepen- dently, but provided some useful insights when combined with other data. Our phylogeny corroborated the monophyly of most groups proposed on the basis of morphology and showed the fossil Palaeovespa is distantly related to extant genera. Unstable relationships among genera suggest that rapid radiations occurred in the early history of the Vespinae. © The Willi Hennig Society 2015. Introduction 2012). With the introduction of geometric morphomet- rics (Rohlf and Marcus, 1993), the study of wing vena- Wing venation is one of the main characters used to tion has been developed further. Wing shape, identify and to classify insects (Comstock and Need- quantified by landmarks at vein intersections, was ham, 1899; Wheeler et al., 2001; Sharkey and Roy, found to be distinct between numerous genera, species 2002; Trautwein et al., 2012). As one of the best- and even isolated populations (e.g. Baylac et al., 2003; preserved structures in fossil insects, it is a crucial fea- Camara et al., 2006; Villemant et al., 2007). Wing ture in understanding insect evolution (Grimaldi and shape also presented a significant phylogenetic signal Engel, 2005; Nel et al., 2012). As such, it has been in different groups, when compared to phylogenies widely used in phylogenetic analyses (e.g. Bybee et al., based on other characters (Klingenberg and Gidas- 2008). Even in the phylogenomic era, it can still pro- zewski, 2010; Bai et al., 2011; Perrard et al., 2014). vide information for countless taxa, including those However, landmark data of the wings have seldom for which no molecular data can be readily obtained, been used in phylogenetic analyses (but see Baracchi such as rare species and fossils (Trautwein et al., et al., 2011; for use of UPGMA). In a case study of the Drosophila melanogaster subgroup, Klingenberg *Corresponding author: and Gidaszewski (2010) reported low homoplasy of Email address: [email protected] wing shapes based on landmark data. On the one © The Willi Hennig Society 2015 2 A. Perrard et al. / Cladistics 0 (2015) 1–20 hand, the topology recovered from morphometric data LAUP minimizes the landmark displacement along a was inconsistent with well-supported molecular phylo- given tree, Catalano and Goloboff (2012) designed a genies, suggesting that wing shape alone may be insuf- new kind of landmark superimposition based on this ficient to estimate a reliable phylogeny (Klingenberg same criterion. This parsimonious alignment takes the and Gidaszewski, 2010). On the other hand, a simulta- topology into account and can occur simultaneously neous analysis of wing landmarks combined with other with the tree search to optimize the alignment, and characters may accentuate the phylogenetic signal of thus the tree inference. The LAUP method presents wing shape while reducing the influence of its homo- two main advantages over previous methods used to plasy on the results (Nixon and Carpenter, 1996). infer phylogenies from landmark data: landmark con- The use of shape data to infer phylogenies has long figurations are treated in an evolutionary context, in been debated (e.g. Bookstein, 1994; Rohlf, 1998; which homologous changes are explicitly identified as Gonzalez-Jos e et al., 2008; Catalano et al., 2010; landmark displacements; and landmark characters can Adams et al., 2011). The shape assessed by geometric be treated simultaneously with other types of charac- morphometrics is a spatial description of a structure ters during a tree search. In addition, landmark loca- excluding information on size, location and orienta- tions are treated as multivariate characters, so the tion. Shape data are inherently continuous and multi- method should be independent from the coordinate variate, thus not easily compatible with most system, like other methods of shape analysis (Catalano phylogenetic frameworks designed for independent, et al., 2010). For these reasons, LAUP was the most univariate, discrete characters (e.g. Bookstein, 1994; relevant method to test the use of wing shape data in Monteiro, 2000). Some attempts to treat geometric phylogenetic analyses. morphometric data as phylogenetic characters have The use of wing landmarks in phylogenetic recon- been made (e.g. Zelditch et al., 1995; Caumul and struction was tested on the subfamily Vespinae, which Polly, 2005; Gonzalez-Jos e et al., 2008) and heavily includes hornets and yellow jackets. This subfamily of criticized (Adams and Rosenberg, 1998; Monteiro, social wasps is relatively small (70 extant species; see 2000; Adams et al., 2011). Recently, a new method of Archer, 2012; Carpenter et al., 2015), thus enabling a “landmark analysis under parsimony” (here abbrevi- fairly comprehensive taxon sampling. The presence of ated as LAUP) has been proposed to treat landmark a phylogenetic signal in the wing shapes was already configurations, a set of landmarks each defined by two confirmed in this group (Perrard et al., 2014). Finally, (2D) or three (3D) coordinates, as such in cladistic several datasets of molecular and morphological char- analyses (Catalano et al., 2010; Goloboff and Cata- acters were available for many species (Carpenter and lano, 2011). This method minimises landmark displace- Perera, 2006; Saito and Kojima, 2011; Perrard et al., ments along the branches of a tree through 2013; Lopez-Osorio et al., 2014). However, these previ- reconstruction of ancestral landmark locations, extend- ous phylogenetic studies had certain limitations: they ing the application of parsimony to landmark configu- did not focus on the entire subfamily; genus-level rela- ration data. tionships were poorly supported; and fossils were not The LAUP method lies outside of the “Procrustes included. Therefore, further analysis of the phylogeny paradigm”, currently used in most geometric morpho- of the group was necessary (Perrard et al., 2013; metric analyses (Zelditch et al., 2012; Adams et al., Lopez-Osorio et al., 2014). 2013). Although Procrustes methods analyse the varia- In this study, we analysed the potential of quan- tion of all landmarks at once, LAUP is based on the tification of the wing venation pattern as a phyloge- sum of individual landmark’s variation first analysed netic character, using LAUP, to help resolve the separately. Geometric morphometrics relies on the phylogeny of vespine wasps. Using a combined anal- notion of a shape-space, a space describing all poten- ysis of traditional morphological data and sequences tial shapes defined by a same number of landmarks. from nine genes, we produced a phylogenetic frame- Procrustes distance is considered the natural metric of work to study the evolution of the subfamily. this space, because it is invariant to the landmark dis- Because LAUP is a new method that has not seen placed and to the orientation of this displacement much use, we first tested its sensitivity to several (Bookstein, 1991). The analysed shapes are usually parameters, using data simulated under a Brownian- superimposed using a Generalized Procrustes Analysis, motion model with a known topology. We then which is designed to minimize the Procrustes distances compared the phylogenetic information of the wing between landmark configurations through a least- landmarks to the results obtained from other types squares approach. With this method, the variation of of data. Finally, we tested whether the wing land- each landmark is spread over the entire configuration: marks improved or misled the phylogeny based on the variation of a single landmark is thus meaningless, morphology, compared to an analysis including tra- making this alignment unsuitable for LAUP. Because ditional wing characters. A. Perrard et al. / Cladistics 0 (2015) 1–20 3 Material and methods Each gene was aligned separately using MAFFT with the L-INS-i algorithm (Katoh et al., 2005). The Phylogeny aligned sequences were concatenated into a mitochon- drial dataset (12S, 16S, COI, COII, Cytb), a nuclear Phylogenetic relationships were