Towards a phylogeny‐based natural classification scheme for Orthoptera

This work represents the most comprehensive phylogenetic analysis of Orthoptera to date (Fig. 9) and presents an excellent opportunity to test previous hypotheses about the phylogenetic relationships among the major lineages within the order. Below, we comment on the higher‐level relationships, which we can confidently resolve using the current data and we propose a new phylogeny‐based natural classification scheme for Orthoptera (Table 5).

Table 5. A phylogeny‐based natural classification scheme proposed in this study Suborder Infraorder Superfamily group Superfamily Included families (alphabetical) Number of described species (extant) ENSIFERA Gryllidea Grylloideaa Gryllidae 4886 Gryllotalpoideab Gryllotalpidae, Mogoplistidae, Myrmecophilidae 547 Tettigoniidea Schizodactyloidea Schizodactylidae 15 Tettigonioidea Tettigoniidaec 7104 Rhaphidophoroidea Rhaphidophoridae 645 Stenopelmatoidea Anostostomatidaed , Gryllacrididae, Stenopelmatidae 913 Hagloidea Prophalangopsidae 8 CAELIFERA Tridactylidea Tridactyloidea Cylindrachetidae, Ripipterygidae, Tridactylidae 205 Acrididea Tetrigoidea Tetrigidae 1763 Acridomorpha Proscopioidea Proscopiidae 214 Eumastacoidea Chorotypidae, Episactidae, Eumastacidae, Euschmidtiidaee , 1008 Mastacideidaee , Morabidae, Thericleidae Tanaoceroidea Tanaoceridae 3 Pneumoroidea Pneumoridae 17 Trigonopterygoidea Trigonopterygidae, Xyronotidae 21 Pyrgomorphoidea Pyrgomorphidae 473 Acridoidea Acrididae, Derycorythidaee , Lathiceridaee , Lentulidae, Lithidiidae, Ommexechidae, Pamphagidae, Pamphagodidae, Pyrgacrididae, Romaleidae, Tristiridae 7976

Figure 9 Open in figure viewer PowerPoint A summary phylogeny of Orthoptera based on ML analysis of total evidence data. For readability, terminals are not shown, but branches are colour coded to show their superfamily identity. Superfamily names used in this figure follow the proposed classification scheme in the present study.

The phylogeny of Ensifera has been contentious over the years and numerous hypotheses have been proposed based on different character systems (Ander, 1939; Zeuner, 1939; Judd, 1947; Blackith and Blackith, 1968; Sharov, 1968; Ragge, 1977; Gorochov, 1995a; Gwynne, 1995; Desutter‐Grandcolas, 2003; Jost and Shaw, 2006). Our total evidence phylogeny (Fig. 5) finds that Ensifera is mainly divided into two groups, one consisting of Grylloidea sensu Gorochov (1995b) and the other consisting of Schizodactyloidea sensu Kevan (1982), Hagloidea sensu Kevan (1982), Rhaphidophoroidea sensu Kevan (1982), Stenopelmatoidea sensu Kevan (1982), and Tettigonioidea sensu Kevan (1982). Although the internal relationships differ, this grouping is similar to the hypothesis proposed by Ander (1939) and corresponds to the infraorders Gryllidea sensu Vickery (1977) and Tettigoniidea sensu Vickery (1977). Within the infraorder Gryllidea, we have recovered Gryllidae (crickets) as sister to a clade consisting of Gryllotalpidae (mole crickets), Mogoplistidae (scaly crickets), and Myrmecophilidae (ant‐loving crickets). The close relationship between Gryllidae and Gryllotalpidae has always been supported by previous studies (Ander, 1939; Zeuner, 1939; Judd, 1947; Sharov, 1968; Vickery, 1977), but their relationship with respect to the other two families has not been resolved because they have sometimes been included as subfamilies of Gryllidae (Rehn and Hebard, 1912). Our phylogeny strongly suggests that Mogoplistidae and Myrmecophilidae form a clade, which is in turn sister to Gryllotalpidae. The clade formed by these three families is quite divergent from Gryllidae. Furthermore, many lineages within Gryllidae are also very divergent from each other, reflecting the ancient age of the group, and it may be reasonable to elevate some of the gryllid subfamilies to the family level, given more thorough analyses with more taxon sampling in the future. In recognition of the two deeply divergent clades within Gryllidea, we propose recognition of two superfamilies within the infraorder, Grylloidea, which includes Gryllidae and Gryllotalpoidea, which includes the remaining three families. As our taxon sampling for Gryllidea is relatively weak compared with other groups included in this study, additional sampling may be necessary to test this hypothesis, but an independent analysis using a larger taxon sampling finds a similar relationship (Chintauan‐Marquier et al., 2015), lending further support for this taxonomic change.

Within Tettigoniidea, we find a basal position of Schizodactyloidea, which comprises a small relict family Schizodactylidae (sand crickets), which is a novel hypothesis. The phylogenetic position of Schizodactyloidea within Ensifera has not been clear (Heads and Leuzinger, 2011). Jost and Shaw (2006), Legendre et al. (2010), as well as our mtgenome analysis, found it to be sister to Gryllidea, while other morphology‐based studies placed them near Tettigoniidea (Ander, 1939; Gorochov, 1995a; Desutter‐Grandcolas, 2003). Heads and Leuzinger (2011) supported a sister relationship between Schizodactyloidea and Gryllidea, which was first proposed by Gwynne (1995), but it was not based on a formal cladistic analysis. Upon close examination of our data, we find that the branch lengths of the members of Gryllidea are exceptionally long and it is possible that our mtgenome analysis may have been affected by long‐branch attraction (Felsenstein, 1978; Bergsten, 2005), meaning that the resulting topology may be an analytical artefact, rather than an accurate relationship. The larger taxon and character sampling of the total evidence analysis seems to have overcome this issue.

We then recover a sister relationship between Tettigonioidea and the remaining three monophyletic superfamilies (Hagloidea, Rhaphidophoroidea, and Stenopelmatoidea). Many of the earlier taxonomists have considered Tettigonioidea and Hagloidea to be closely related because these are the only two superfamilies outside Gryllidea that emit sounds with a tegminal design and hear with tibial tympanal structures (Ander, 1939; Zeuner, 1939; Ragge, 1955; Gwynne, 1995; Desutter‐Grandcolas, 2003). However, it is important to recognize that many ensiferans within Tettigoniidea can also produce femoro‐abdominal stridulation, which can be perceived by either membranous tympana or mechanoreceptors (Desutter‐Grandcolas, 2003). Tettigonioidea includes the most diverse and speciose orthopteran family, Tettigoniidae (katydids), which has the stridulatory file on the left tegmen (Gwynne, 2001), and Hagloidea, which includes only a single extant family, Prophalangopsidae (ambidextrous crickets), and numerous extinct families, all of which have stridulatory files on both tegmina (Spooner, 1973). Jost and Shaw (2006) proposed a more radical scheme, which placed Hagloidea (represented by Cyphoderris only) as the most basal lineage within Ensifera and suggested that acoustic communication is the ancestral condition for Ensifera and has been lost multiple times. Recently, Zhou et al. (2014) suggested a sister relationship between Hagloidea and Rhaphidophoroidea based on mtgenome data, but the study lacked robust taxon sampling because it included only one species per superfamily and did not include the members of Stenopelmatoidea. Our study finds a novel relationship and does not find support for the sister relationship between Tettigonioidea and Hagloidea, or the sister relationship between Hagloidea and Rhaphidophoroidea, or the basal placement of Hagloidea. Instead, we find the clade (Rhaphidophoroidea (Hagloidea + Stenoplematoidea)), which is, in turn, sister to Tettigoniidae. The acoustic communication is certainly a very complex syndrome that can be achieved from diverse ways of producing sound and equally diverse ways of perceiving sound (Desutter‐Grandcolas, 2003) and it is not well justified to treat it as a simple binary character to test whether it is ancestral or derived. A more appropriate way is to conduct a detailed anatomical study to carefully form homology statements of various components of sound production and hearing to optimize on to the phylogeny. Thus, a study with larger taxon sampling and detailed morphological analyses is necessary to fully understand the evolution of acoustic communication in these insects.

Recently, Heller et al. (2014) elevated the status for the tettigoniid subfamily Phaneropterinae to full family Phaneropteridae, which includes four plant‐feeding subfamilies, Phaneropterinae, Pseudophyllinae, Mecopodinae, and Phyllophorinae, based on a recent molecular study by Mugleston et al. (2013) and a previous hypothesis by Gorochov (1995b). This taxonomic change implies that Phaneropteridae as a whole is a monophyletic group, but Mugleston et al. (2013) found that one of the pseudophylline tribes, Pterochrozini, did not group with other pseudophyllines, but was placed at the base of katydid phylogeny, thereby rendering the concept of Phaneropteridae paraphyletic. Our study is built upon the data generated by Mugleston et al. (2013), and we also do not find strong support for the family Phaneropteridae. To make matters worse, Gorochov (2012) elevated several tribes within Pseudophyllinae to subfamilies and created a “subfamily group” Pseudophyllidae, but this hypothesis has not been fully tested. The katydid classification is clearly in a state of flux and a major revision of the classification will be required once a definitive phylogeny of Tettigoniidae becomes available. Thus, in this study, we recognize a single family, Tettigoniidae, that has always been found monophyletic.

Our study proposes a novel phylogenetic position for Rhaphidophoroidea, which includes a single cosmopolitan family Rhaphidophoridae (camel crickets). Gorochov (2001) considered Rhaphidophoridae as a member of Stenopelmatoidea, but our study shows that it is divergent from Stenopelmatoidea. Likewise, a sister relationship between Stenopelmatoidea and Hagloidea is also novel. Although our analysis based on the mtgenome finds only paraphyletic Stenopelmatoidea, the total evidence analysis (Fig. 5) based on more taxon sampling strongly recovers the monophyly of the superfamily consisting of Anostostomatidae (wetas and king crickets), Stenopelmatidae (Jerusalem crickets), and Gryllacrididae (raspy crickets and leaf‐rolling crickets). Anostostomatidae is found to be paraphyletic with respect to Cooloolidae (cooloola monsters), but evidence suggests that Cooloolidae are actually aberrant Anostostomatidae, and Gorochov (2001) also expressed this view. However, more taxon sampling is required to fully resolve the relationships among Rhaphidophoroidea, Stenopelmatoidea, and Hagloidea, and allow the definition of monophyletic units of evolution for extant taxa and fossils.

We now have a very clear understanding of the phylogeny of Caelifera and the relationships among superfamilies. Like Ensifera, Caelifera is mainly divided into two infraorders, Tridactylidea sensu Kevan (1982), which comprises a single superfamily, Tridactyloidea, and Acrididea sensu Kevan (1982), which includes all the other caeliferan superfamilies (Fig. 5). Previous molecular phylogenetic hypotheses of Caelifera (Flook and Rowell, 1997; Flook et al., 1999; Leavitt et al., 2013; Zhang et al., 2013a,b) consistently recovered the basal position of Tridactyloidea sensu Dirsh (1975), followed by Tetrigoidea sensu Dirsh (1975), and our study also confirms this hypothesis. Although some earlier studies focusing on the fossil evidence proposed a sister relationship between Tridactyloidea and Tetrigoidea (Ragge, 1955; Sharov, 1968), other morphologists thought that Tetrigoidea was more closely related to other caeliferan superfamilies (Dirsh, 1975; Kevan, 1982; Vickery, 1997) and our study concurs with the latter. Tridactyloidea is the earliest branch within Caelifera, currently consisting of three families, Tridactylidae (pygmy mole crickets), the Neotropical relative Ripipterygidae, and the subterranean Cylindrachetidae (sandgropers). Although Vickery (1997) considered Cylindrachetidae to form its own superfamily, Cylindrachaetoidea, Flook and Rowell (1997) included it within Tridactyloidea and our findings support this position. The infraorder Acrididea consists of Tetrigoidea and Acridomorpha, the former comprised of a single cosmopolitan family, Tetrigidae (pygmy grasshoppers and grouse locusts), which is characterized by the extension of the pronotum over the entire dorsal surface of the abdomen (Kevan, 1982). The latter is a group of seven superfamilies collectively known as Acridomorpha for their grasshopper‐like morphology and herbivorous feeding habit (Dirsh, 1975; Flook and Rowell, 1997; Song, 2010). The higher‐level classification within Acridomorpha has been largely informed by male phallic structures (Dirsh, 1973; Amédégnato, 1974; Eades, 2000; Song, 2010), but individual taxonomists have interpreted these morphological characters differently from each other, resulting in several conflicting schemes (Song, 2010). Molecular data have been very useful in resolving these conflicts (Flook and Rowell, 1997; Flook et al., 1999, 2000; Leavitt et al., 2013). Recently, Song and Mariño‐Pérez (2013) compared the phylogenetic signal in male phallic structures with that of molecular data, and showed that many traditionally used characters are highly homoplasious, while some phallic structures do have a strong signal. The present study is largely congruent with the previous molecular studies (Flook and Rowell, 1997; Flook et al., 1999, 2000; Leavitt et al., 2013) and clarifies some of the conflicts from the earlier taxonomic work.

In this study, we find that Acridomorpha is divided into two groups: Proscopioidea sensu Descamps (1973b) + Eumastacoidea sensu Descamps (1973b) and the clade consisting of the remaining five superfamilies. Proscopioidea comprises a single family Proscopiidae (jumping sticks). Although this phasmid‐looking grasshopper family has sometimes been considered a member of Eumastacoidea (Dirsh, 1961, 1975), we consider it here as a separate superfamily based on its unique apomorphies (Descamps, 1973a,b) as well as its robust basal position relative to other eumastacoids. Our study clarifies the ambiguous position of Proscopioidea as found by Matt et al. (2008). Eumastacoidea includes seven families (Eades et al., 2014) that are commonly referred to as monkey grasshoppers. Of the remaining five superfamilies within Acridomorpha, the earliest diverging lineage is Tanaoceroidea sensu Kevan (1982), which includes a small relict family Tanaoceridae, known only from three species endemic to the southwestern USA, and characterized by extremely long antennae and a rudimentary male phallic complex (Rehn, 1948; Dirsh, 1955; Grant and Rentz, 1967).

Then the lineage is divided into two clades, one consisting of Pneumoroidea sensu Flook et al. (2000) and Trigonopterygoidea sensu Flook et al. (2000) and the other consisting of Pyrgomorphoidea sensu Flook et al. (1999) and Acridoidea sensu Flook et al. (2000). Pneumoroidea contains one family, Pneumoridae (bladder grasshoppers, flying gooseberries), and 17 described species mostly found in South Africa, and is known for its femoro‐abdominal stridulatory mechanism (Dirsh, 1965). Trigonopterygoidea consists of two rather divergent families, Trigonopterygidae and Xyronotidae. The former is endemic to Southeast Asia, contains 17 species, and is characterized by reversed male genitalia and foliaceous tegmina (Dirsh, 1952). The latter contains four species endemic to central Mexico and can be characterized by rudimentary male genitalia and a stridulatory ridge on the third abdominal tergite (Dirsh and Mason, 1979). Flook et al. (2000) recovered these two families as a monophyletic group and our study corroborates their findings. However, the sister relationship between Pneumoroidea and Trigonopterygoidea is novel. Dirsh and Mason (1979) considered Tanaoceridae, Pneumoridae, and Xyronotidae to form a monophyletic lineage because of the apparently shared femoro‐abdominal stridulatory mechanism, but Flook et al. (2000) thoroughly showed that this morphological trait must have evolved multiple times within the basal caeliferans and our findings bolster this idea.

Pyrgomorphoidea includes a single family, Pyrgomorphidae (gaudy grasshoppers), that contains about 470 species distributed globally, with most of its diversity found in the Old World, and is characterized by the presence of a groove in the fastigium (Kevan and Akbar, 1964). Members of this family are often large, strikingly coloured, and known to feed on toxic plants for their defense (Rowell, 1967; Chapman et al., 1986; Whitman, 1991). Dirsh (1975) placed the family Pamphagidae within Pyrgomorphoidea based on the similarity of male phallic structures, but our study clearly shows that Pyrgomorphidae alone forms a distinct sister lineage to Acridoidea, and Pamphagidae is firmly included within Acridoidea, which corroborates the earlier findings by Flook and Rowell (1997) and Flook et al. (1999).

Finally, Acridoidea is the largest superfamily within Acridomorpha, and currently includes 11 recognized families and more than 7900 described species, which are defined by the morphology of the male phallic complex and the lack of a basioccipital slit, among other characters (Roberts, 1941; Chopard, 1949; Dirsh, 1973; Amédégnato, 1974; Kevan, 1982; Eades, 2000). Many species in this group can be recognized as typical and familiar grasshoppers. Within Acridoidea, we find that Pyrgacrididae, which is endemic to Réunion Island in the Indian Ocean (Hugel, 2005), is the earliest diverging lineage, representing a transitional form between Pyrgomorphoidea and Acridoidea (Eades, 2000). Leavitt et al. (2013) found Pamphagidae + Pamphagodidae to be the basal lineage within Acridoidea, but their nodal support for the backbone relationships was poor. The present study is based on large taxon and character sampling and our nodal support is much stronger than that of Leavitt et al. (2013).