Phylogeny of the Neuropterida (Insecta: Holometabola)

The Neuropterida, with about 6500 known species — living fossils in a way — at the base of the Holometabola (as a sister group of the Coleoptera), comprise Raphidioptera (about 210 species, two families), Megaloptera (about 300 species, two families) and Neuroptera (6000 species, 17 families). Megaloptera + Neuroptera is argued vs. the traditional Raphidioptera + Megaloptera. Raphidioptera are undisputedly monophyletic. Monophyly of Megaloptera is the operational hypothesis, although occasionally questioned. Sucking tubes of the larvae are the most spectacular autapomorphy of Neuroptera. The construction of larval head capsules indicates three evolutionary lines: Nevrorthiformia, and Myrmeleontiformia + Hemerobiiformia. Traditional Myrmeleontiformia is Psychopsidae + (Nemopteridae + (Nymphidae + (Myrmeleontidae + Ascalaphidae))), the present approach is (Psychopsidae + Nemopteridae) + all other Myrmeleontiformia. Hemerobiiformia are based on the ‘maxillary head’ concept. The ithonid clade Ithonidae/Rapismatidae + Polystoechothidae and the dilarid clade Dilaridae + (Mantispidae + (Rhachiberothidae + Berothidae)) are based on robust criteria. Other relationships remain unclear: Hemerobiidae + Chrysopidae (on similarity) and the ‘early offshoot’ concept of coniopterygidae (on autapomorphies) should not be perpetuated. Chysopidae + Osmylidae and (Hemerobiidae + (Coniopterygidae + Sisyridae)) + dilarid clade are discussed. Aquatic larvae, regarded as independent apomorphies of megaloptera and neuropteran Nevrorthidae and Sisyridae for a long time, are re‐interpreted as a synapomorphy of Megaloptera + Neuroptera and thus plesiomorphic within these groups. Terrestrial larvae (with cryptonephry to solve osmotic problems) are consequently apomorphic. Aquatic Sisyridae with cryptonephry of a single malpighian tubule, is conflicting, but larvae may have become secondarily aquatic, after a terrestrial intermezzo.     

Phylogeny of the Neuropterida: a first molecular approach

Abstract. In a first molecular approach specially dedicated to examining the phylogeny of the Neuropterida, two nuclear and two mitochondrial genes were tested: 18S rRNA, translation elongation factor‐1α, cytochrome c oxidase subunit 3 and 16S rRNA. Molecular results are discussed in the light of a previous holomorphological cladistic analysis. The hypothesis of a sister‐group relationship Raphidioptera + (Neuroptera + Megaloptera) put forward in recent morphological analyses is supported by our data, which is in contrast to the traditional view (Raphidioptera + Megaloptera) + Neuroptera. Furthermore, the Nevrorthidae (constituting the suborder Nevrorthiformia) as a sister group of all other Neuroptera is confirmed. The disruption of the suborder Hemerobiiformia is the most conflicting result of the molecular analysis. Sisyridae and Osmylidae do not cluster within Hemerobiiformia, but represent two distinct and widely separated branches. The remaining Hemerobiiformia emerge as the sister group of the suborder Myrmeleontiformia, which is once more confirmed as monophyletic. Among the genes tested, cytochrome c oxidase subunit 3 proved to be most potent for resolving the phylogenetic relationships among Neuropterida. The nuclear gene for the ribosomal 18S rRNA is too conserved within the alignable regions, whereas the variable sections are too divergent to be applicable within this evolutionary time frame. The elongation factor‐1α gene proved to exist in more than one copy in Neuropterida, and thus is not applicable in the present state of knowledge. With respect to the mitochondrial sequences (cytochrome c oxidase subunit 3, 16S rRNA), saturation impedes the unambiguous resolution of deeper nodes. Apparently, due to early diversification of the heterogeneous Neuroptera, phylogenetic analysis of this group remains a challenge with respect to selection of the proper genes and mutatis mutandis the morphological approach.     

Phylogenetic relevance of the genital sclerites of Neuropterida (Insecta: Holometabola)

Abstract Segment 9 of male Raphidioptera, comprising tergite, sternite, gonocoxites, gonostyli and gonapophyses, is a benchmark for homologies in the male and female terminalia of the three Neuropterida orders Raphidioptera, Megaloptera and Neuroptera. The segments relating to genitalia are 9, 10 and 11 in males and 7, 8 and 9 in females. Results from holomorphological and recent molecular cladistic analyses of Neuropterida agree in supporting the sister‐group relationships between: (1) the Raphidioptera and the clade Megaloptera + Neuroptera, and (2) the suborder Nevrorthiformia and all other Neuroptera. The main discrepancy between the results of these studies is the nonmonophyly of the suborder Hemerobiiformia in the molecular analysis. The monophyly of the Megaloptera (which has been repeatedly questioned) is further corroborated by a hitherto overlooked ground pattern autapomorphy: the presence of eversible sacs within the complex of the fused gonocoxites 11 in Corydalidae and Sialidae. The recently discovered paired complex of gonocoxites 10 (parameres) in Nipponeurorthus (Nevrorthidae) indicates that the curious apex of sternite 9 of Nevrorthus and Austroneurorthus is the amalgamation of the sclerites of gonocoxites 10 with sternite 9, interpreted as synapomorphic. In the molecular study, the Nevrorthidae, Sisyridae and Osmylidae branch off in consecutive splitting events, a result that is supported by the analysis of male genital sclerites reported here. Extraordinary parallel apomorphies (e.g. excessive enlargement and modification of gonocoxites 10 ending in a thread‐like ‘penisfilum’) in derived representatives of Coniopterygidae, Berothidae, Rhachiberothidae and Mantispidae corroborate the dilarid clade of the morphological analysis and leads us to hypothesize a sister‐group relationship of the Coniopterygidae with the dilarid clade. A re‐interpretation of the tignum of Chrysopidae as gonocoxites 11 means that the structure previously called the gonarcus represents the fused gonocoxites 9. In Hemerobiidae, the corresponding sclerite is consequently also homologized as fused gonocoxites 9. The enlargement of the lateral wings of the gonocoxites in both families is interpreted as a synapomorphy. Excessive enlargement of gonostyli 11 in the Polystoechotid clade and Myrmeleontiformia supports a sister‐group relationship of these two clades. The occurrence of certain serial homologues of female genitalia structures (gonocoxites and gonapophyses), such as the digitiform processus together with the flat appendices in segment 8 of certain Myrmeleontidae, or the wart‐like processus together with the flat circular sclerites in segment 7 of certain Berothidae, as well as the presence of gonocoxites 8 as pseudosternites in certain Nemopteridae and Coniopterygidae, are probably character reversals. The digitiform processus of tergite 9 (pseudogonocoxites) in Rhachiberothidae and Austroberothella (Berothidae) are either independently developed acquisitions with a function in oviposition, or are homologous sclerites, possibly of epipleurite origin.     

Mitochondrial phylogenomics illuminates the evolutionary history of Neuropterida

Neuroptera (lacewings) and allied orders Megaloptera (dobsonflies, alderflies) and Raphidioptera (snakeflies) are predatory insects and together make up the clade Neuropterida. The higher‐level relationships within Neuropterida have historically been widely disputed with multiple competing hypotheses. Moreover, the evolution of important biological innovations among various Neuropterida families, such as the origin, timing and direction of transitions between aquatic and terrestrial habitats of larvae, remains poorly understood. To investigate the origin and diversification of lacewings and their allies, we undertook phylogenetic analyses of mitochondrial genomes of all families of Neuropterida using Bayesian inference, maximum likelihood and maximum parsimony methods. We present a robust, fully resolved phylogeny and divergence time estimation for Neuropterida with strong statistical support for almost all nodes. Mitochondrial sequence data are typified by significant compositional heterogeneity across lineages, and parsimony and models assuming homogeneous rates did not recover Neuroptera as monophyletic. Only a model accounting for compositional heterogeneity (i.e. CAT‐GTR) recovered all orders of Neuropterida as monophyletic. Significant findings of the mitogenomic phylogeny include recovering Raphidioptera as sister to Megaloptera plus Neuroptera. The sister family of all other lacewings are the dusty‐wings (Coniopterygidae), rather than Nevrorthidae. Nevrorthidae are instead returned to their traditional position as the sister group of the spongilla‐flies (Sisyridae) and closely related to Osmylidae. Our divergence time analysis indicates that the Mesozoic was indeed a ‘golden age’ for lacewings, with most families of Neuropterida diverging during the Triassic and Jurassic and all extant families present by the Early Cretaceous. Based on ancestral character state reconstructions of larval habitat we evaluate competing hypotheses regarding the life style of early neuropteridan larvae as either aquatic or terrestrial.     

The larval head of Nevrorthidae and the phylogeny of Neuroptera (Insecta)

External and internal head structures of larvae of Nevrorthidae were described in detail. The results were compared to conditions found in other representatives of Neuroptera and the other two neuropterid orders. The cladistic analysis supported the monophyly of Neuroptera, Neuroptera exclusive of Nevrorthidae, Hemerobiiformia, and Myrmeleontiformia. Neuroptera exclusive of Nevrorthidae are supported by the formation of an undivided postmentum and the presence of cryptonephric Malpighian tubules. The highly specialized articulation of the neck (Rollengelenk) and the absence of a salivary duct are autapomorphies of Nevrorthidae. Ithonidae and Polystoechotidae form a clade and are the sister group of the remaining Hemerobiiformia, which are characterized by the complete lack of a gula and a terminal filament of the antenna. Within this lineage, a clade comprising Mantispidae, Dilaridae, Berothidae, and Rhachiberothidae is well supported. Larvae of Myrmeleontiformia are characterized by a complex transformation of head structures, with a hypostomal bridge, a small triangular gula, largely reduced maxillary grooves, and anteriorly shifted posterior tentorial grooves. The slender finger‐like mid‐dorsal apodeme is another autapomorphy of the group. Psychopsidae are placed as the sister group of the remaining Myrmeleontiformia, which are characterized by a conspicuous, protruding ocular region (often less distinct or even absent in Nemopteridae). Ascalaphidae are the sister group of Myrmeleontidae. Larvae of both families share the fusion of the tibia and tarsus in the hind leg. The larval characters analysed were not sufficient for full resolution of the myrmeleontiform and hemerobiiform lineages. The position of several families such as Osmylidae, Sisyridae, and Coniopterygidae remains uncertain. The results are in agreement with an aquatic ancestor of Neuroptera and secondarily acquired terrestrial habits within the lineage (Neuroptera exclusive of Nevrorthidae), and another invasion of the aquatic environment by Sisyridae. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158 , 533–562.     

Wing Base Structural Data Support the Sister Relationship of Megaloptera and Neuroptera (Insecta: Neuropterida)

The phylogenetic status and the monophyly of the holometabolous insect order Megaloptera has been an often disputed and long unresolved problem. The present study attempts to infer phylogenetic relationships among three orders, Megaloptera, Neuroptera, and Raphidioptera, within the superorder Neuropterida, based on wing base structure. Cladistic analyses were carried out based on morphological data from both the fore- and hindwing base. A sister relationship between Megaloptera and Neuroptera was recovered, and the monophyly of Megaloptera was corroborated. The division of the order Megaloptera, the traditional higher classification, into Corydalidae (Corydalinae + Chauliodinae) and Sialidae, was also supported by our wing base data analyses.     

Phylogeny of Myrmeleontiformia based on larval morphology (Neuropterida: Neuroptera)

The suborder Myrmeleontiformia is a derived lineage of lacewings (Insecta: Neuroptera) including the families Psychopsidae, Nemopteridae, Nymphidae, Ascalaphidae and Myrmeleontidae. In particular, Myrmeleontidae (antlions) are the most diverse neuropteran family, representing a conspicuous component of the insect fauna of xeric environments. We present the first detailed quantitative phylogenetic analysis of Myrmeleontiformia, based on 107 larval morphological and behavioural characters for 36 genera whose larvae are known (including at least one representative of all the subfamilies of the suborder). Four related families were used as outgroups to polarize character states. Phylogenetic analyses were conducted using both parsimony and Bayesian methods. The reconstructions resulting from our analyses corroborate the monophyly of Myrmeleontiformia. Within this clade, Psychopsidae are recovered as the sister family to all the remaining taxa. Nemopteridae (including both subfamilies Nemopterinae and Crocinae) are recovered as monophyletic and sister to the clade comprising Nymphidae + (Myrmeleontidae + Ascalaphidae). Nymphidae consist of two well‐supported clades corresponding to the subfamilies Nymphinae and Myiodactylinae. Our results suggest that Ascalaphidae may not be monophyletic, as they collapse into an unresolved polytomy under the Bayesian analysis. In addition, the recovered phylogenetic relationships diverge from the traditional classification scheme for ascalaphids. Myrmeleontidae are reconstructed as monophyletic, with the subfamilies Stilbopteryginae, Palparinae and Myrmeleontinae. We retrieved a strongly supported clade comprising taxa with a fossorial habit of the preimaginal instars, which represents a major antlion radiation, also including the monophyletic pit‐trap building species.     

The function and phylogenetic implications of the tentorium in adult Neuroptera (Insecta)

Despite several recent analyses on the phylogeny of Neuroptera some questions still remain to be answered. In the present analysis we address these questions by exploring a hitherto unexplored character complex: the tentorium, the internal cuticular support structure of the insect head. We described in detail the tentoria of representatives of all extant neuropteran families and the muscles originating on the tentorium using 3D microCT images and analyzed differences in combination with a large published matrix based on larval characters. We find that the tentorium and associated musculature are a source of phylogenetically informative characters. The addition of the tentorial characters to the larval matrix causes a basad shift of the Sisyridae and clearly supports a clade of all Neuroptera except Sisyridae and Nevrorthidae. A sister group relationship of Coniopterygidae and the dilarid clade is further corroborated. A general trend toward a reduction of the dorsal tentorial arms and the development of laminatentoria is observed. In addition to the phylogenetic analysis, a correlation among the feeding habits, the development of the maxillary muscles, and the laminatentoria is demonstrated.