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Phylogenetic Analysis of the Genus Argia Rambur, 1842 (Odonata: Coenagrionidae), Based on Morphological Characters of Larvae and Mitochondrial DNA Sequences

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Phylogenetic Analysis of the Genus Argia Rambur, 1842 (Odonata: Coenagrionidae), Based on Morphological Characters of Larvae and Mitochondrial DNA Sequences Org Divers Evol (2017) 17:409–420 DOI 10.1007/s13127-017-0325-7 ORIGINAL ARTICLE Phylogenetic analysis of the genus Argia Rambur, 1842 (Odonata: Coenagrionidae), based on morphological characters of larvae and mitochondrial DNA sequences Mónica Torres-Pachón1 & Rodolfo Novelo-Gutiérrez1 & Alejandro Espinosa de los Monteros2 Received: 21 September 2016 /Accepted: 27 February 2017 /Published online: 17 March 2017 # Gesellschaft für Biologische Systematik 2017 Abstract The study of the evolutionary interrelationships phylogenies; nonetheless, there is historical congruence among the species encompassed in the Neotropical genus among them. Within Argia, five clades were consistently Argia (Zygoptera: Coenagrionidae) has been neglected. The recovered. Most of those clades have been identified, at least goal of this study is to infer the phylogenetic relationships in part, in previous phylogenetic and taxonomic studies. among 36 species of Argia Rambur, 1842, using complemen- Indubitably, the morphological characters from larvae have tary data sets (i.e., larval morphology and mitochondrial historical signal useful for cladistic and taxonomic inference. DNA). The morphological data set comprises 76% of the Therefore, it should be a priority to pay more attention to this larvae currently described for this genus and includes 97 source of characters. morphological characters. From those, 47 characters have not been previously used in taxonomic studies involving drag- Keywords 16S rRNA . Cytochrome oxidase subunit I . onflies’ larvae. This is the first cladistic study based on larvae Coenagrionidae . Bayesian inference . Larval morphology . morphology for species within the suborder Zygoptera. Data Parsimony . Zygoptera partitions were analyzed individually, as well as total evi- dence, using parsimony and Bayesian inference as criteria for optimal-tree selection. The results support the monophyly Introduction of the North American species of Argia. This genus can be identified by the combination of eight synapomorphies, four Within the order Odonata, Argia is the most diverse genus, of which are exclusively found in Argia. According to the with 128 described species (Garrison and von Ellenrieder optimal trees, the individual data sets (i.e., morphology and 2015; Schorr and Paulson 2016). This genus is distributed DNA sequences) have a high level of homoplasy, resulting in exclusively in the New World, with Mexico as the country soft polytomies and low support for several nodes. The with the largest number of described species (49 spp., corre- specific relationships of the terminal units differ between the sponding to 38.28% of the total species) (González-Soriano and Novelo-Gutiérrez 2007, 2014), relative to the species Electronic supplementary material The online version of this article recorded for Central America (15 spp.), USA (32 spp.), Brazil (doi:10.1007/s13127-017-0325-7) contains supplementary material, (29 spp.), and Colombia (22 spp.) (González-Soriano 2012). which is available to authorized users. Argia was described by Rambur in 1842 with only two species: Argia impura and Argia obscura. The latter was sub- * Alejandro Espinosa de los Monteros sequently considered as a junior synonym of Agrion [email protected] fumipenne (Garrison et al. 2010). To date, some 150 names of species have been proposed. From these, 128 could be 1 Department of Biodiversidad y Sistemática, Instituto de Ecología, A.C., Carretera antigua a Coatepec 351, El Haya, considered valid names (Garrison and von Ellenrieder 2015; 91070 Xalapa, Veracruz, Mexico Schorr and Paulson 2016). 2 Department of Biología Evolutiva, Instituto de Ecología, A.C., Garrison (1994) conducted a synopsis of the species within Carretera antigua a Coatepec 351, El Haya, 91070 Xalapa, Veracruz, the genus Argia for North America and the north of Mexico Mexico and admitted 29 species. However, the species of Mexico, 410 Torres-Pachón M. et al. Central America, and South America need to be reviewed, Phylogenetic studies that have included the genus Argia since several names that appear in the bibliography cannot be associated with any species (Garrison et al. 2010). A number of phylogenetic studies at the level of family, sub- Likewise, the lack of updated keys, the existence of descrip- family, and other genera of the order Odonata have included tions scattered in the bibliography and the lack of illustrations, some species of the genus Argia. The location of these species and the great diversity of species of Argia make the identifi- changed within the topologies of trees according to the traits cation of these species a complex task (Garrison et al. 2010). (i.e., morphological, molecular, or both) and the optimality On the other hand, the taxonomy of larvae is still criteria used (i.e., parsimony, maximum likelihood, and deficient, as only 36% (46 spp.) of the 128 recognized Bayesian inference) (Rehn 2003; Saux et al. 2003; Bybee species are known, with half of these having been et al. 2008; Pessacq 2008;YuandBu2011; von Ellenrieder described over the past 10 years (Pérez-Gutiérrez and 2013;Dijkstraetal.2014). Montes-Fontalvo 2011). Moreover, some of the descrip- In a research on the phylogenetical reassessment of the tions conducted in the first half of the twentieth century Coenagrionidae subfamilies, O’Grady and May (2003) in- lack detailed illustrations of the diagnostic traits, which cluded the species Argia sedula, Argia moesta,andArgia makes them difficult to interpret. bipunctulata in their analysis. As a result, in one of the trees proposed, Argia was recovered as a polyphyletic group. In another phylogenetic tree, Argia was a monophyletic group, Phylogenetic studies including larvae with A. bipunctulata as the basal clade, whereas A. sedula and A. moesta were sister species. Within the order Odonata, the phylogenetic hypotheses have Carle et al. (2008), in a phylogenetic study focused on the been proposed based primarily on morphological traits of superfamily Coenagrionoidea, included the species A. moesta adults (Westman et al. 2000;May2002; Carle and Kjer and Argia vivida. These were not recovered as sister species. 2002; von Ellenrieder 2002, 2013;Rehn2003;O’Grady and A. moesta appeared as a sister taxon of Neoneura May 2003; Pessacq 2008; Yu and Bu 2011;Blankeetal. (Protoneuridae), newly integrated to the Coenagrionidae as 2013) or exclusively on molecular information (Chippindale the subfamily Protoneurinae (Dijkstra et al. 2014). et al. 1999; Misof et al. 2000;Artissetal.2001;Guanetal. In a study on the redefinition of the families in the suborder 2013;Dijkstraetal.2014; Kim et al. 2014), in a few cases on Zygoptera, Dijkstra et al. (2014) included two species of Argia the analysis of a combination of data sets (morphology of (i.e., Argia oculata and Argia sp.), which formed a monophy- adults + larvae + fossils + DNA sequences) (Baskinger et al. letic group and were the sister species of the genera Neoneura, 2008; Bybee et al. 2008; Caesar and Wenzel 2009). However, Epipleoneura,andDrepanoneura. However, the authors studies that explore new morphological traits of larvae (e.g., found that the support values for some coenagrionid groups length and proportion between structures) are scarce. were low and the phylogenetic relationships among them Furthermore, the assessment of those characters in a phyloge- changed if Argia was excluded. As a result, the authors sug- netic contest to diagnose monophyletic clades is a novel gest conducting further phylogenetic studies on this genus and attempt. At the family level, the only works that can be other related genera. mentioned have been conducted with Aeschnidiidae The only preliminary Bayesian inference analysis focused (Odonata: Anisoptera; Fleck et al. 2002), Petaluridae on molecular traits and some morphological features for the (Odonata: Anisoptera; Fleck 2011), and Epiophlebiidae species of Argia living in Northern Mexico was conducted by (Odonata: Anisozygoptera; Blanke et al. 2015). Similarly, Caesar and Wenzel (2009). These authors included in their studies based on the combination of larval morphology and analyses nine morphological traits of adults of both sexes, molecular information include those for Leucorrhinia one trait of larvae, and sequences of the mitochondrial 16S (Odonata: Libellulidae) (Hovmoller and Johansson 2002)and ribosomal RNA (rRNA) gene. These authors reported two Micromacromia (Odonata: Libellulidae) (Fleck et al. 2008). trees based on molecular information alone, which include Phylogenetic hypotheses based solely on traditional three polytomies. The combination of morphological and taxonomic traits of larvae have not been proposed within the molecular data improved the resolution in the topology of suborder Zygoptera. However, Carle and Louton (1994), the third proposed tree, which was the authors’ main phylo- Novelo-Gutiérrez (1995), Ware et al. (2007 ), Caesar and genetic hypothesis. In this phylogeny, the Argia species group Wenzel (2009), Ballare and Ware (2011), and Dijkstra et al. was recovered as monophyletic (Caesar and Wenzel 2009). (2014) stressed the importance of morphological exploration However, the clade formed by Argia nahuana, Argia alberta, of new traits and the use of the traditional taxonomic traits of Argia leonorae, Argia agrioides, Argia hinei, Argia pallens, larvae, as a potential solid source of information to understand Argia fumipennis, A. sedula, Argia pulla,andArgia rhoadsi the evolutionary relationships between the Odonata species displayed
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