Molecular Phylogeny of the Grasshopper Family Pyrgomorphidae

Zootaxa 4969 (1): 101–118 ISSN 1175-5326 (print edition) https://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2021 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4969.1.5 http://zoobank.org/urn:lsid:zoobank.org:pub:DAA2B420-B2E3-45C2-8F6E-33F85857B3FD Molecular phylogeny of the grasshopper family Pyrgomorphidae (Caelifera, Orthoptera) reveals rampant paraphyly and convergence of traditionally used taxonomic characters SUNDUS ZAHID1,2, RICARDO MARIÑO-PÉREZ2,3 & HOJUN SONG2* 1Department of Zoology, Hazara University, Mansehra, Pakistan �[email protected]; https://orcid.org/0000-0001-8986-3459 2Department of Entomology, Texas A&M University, College Station, TX, USA 3Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA �[email protected]; https://orcid.org/0000-0002-0566-1372 *Corresponding author. �[email protected]; https://orcid.org/0000-0001-6115-0473 Abstract The grasshopper family Pyrgomorphidae is one of the most colorful orthopteran lineages, and includes biologically fascinating and culturally important species. Recent attempts to reconstruct the phylogeny of this family have resulted in a large degree of conflicts between a morphology-based study and a molecular-based study, mainly due to convergent morphological traits that affected phylogenetic reconstruction. In this study, a molecular phylogeny of Pyrgomorphidae based on 32 ingroup species and mitochondrial genome data is proposed, which is used to test the monophyly of the taxonomic groupings used in the current classification scheme. Using the ancestral character state reconstruction analyses and character mapping, we demonstrate that some of the morphological characters, including the male genitalia, which were considered to be taxonomically important, have evolved convergently across the phylogeny. We discuss the discrepancies between our phylogeny and the previous studies and propose an approach to establish a natural classification scheme for Pyrgomorphidae. Key word: paraphyly, convergence, male genitalia, mitochondrial genome Introduction The grasshopper family Pyrgomorphidae is among the most recognizable orthopteran lineages in the world. Some members of the family are well known for their vibrant color patterns, elaborate sculptures, and large sizes, which collectively make the common name gaudy grasshoppers quite suitable (Mariño-Pérez & Song, 2018) (Fig. 1). Several of these colorful pyrgomorph species are known to be aposematic and feed on toxic plants (Rowell, 1967; Yang et al., 2019), and capable of sequestering plant secondary metabolites as defensive chemicals by foaming or squirting (Whitman, 1990). Most pyrgomorph species are, however, cryptically colored and not known to be chemically defended (Mariño-Pérez & Song, 2018). Some pyrgomorph species are important agricultural pests that cause considerable economic damages (COPR, 1982) while other species are culturally important as they are consumed by humans (Cerritos & Cano-Santana, 2008). Pyrgomorphidae is characterized by the presence of a groove in the fastigium (Kevan & Akbar, 1964) and distinctive male phallic structures, such as the cingulum extending around to the ventral side, medially directed endophallic apodemes, and the ejaculatory sac opening to the genital chamber (Eades, 2000). Because of these clear morphological synapomorphies, the monophyly of Pyrgomorphidae has not been questioned, and recent phylogenetic studies have consistently demonstrated the monophyly of the family (Eades, 2000; Mariño-Pérez & Song, 2018, 2019; Song et al., 2015; Song et al., 2020). This family is the sole member of the superfamily Pyrgomorphoidea, which is sister to the superfamily Acridoidea (Song et al., 2015; Song et al., 2020). These two superfamilies diverged in the early Cretaceous (Mariño-Pérez & Song, 2019; Song et al., 2020) and the lineage Accepted by D. Rentz: 12 Apr. 2021; published: 10 May 2021 101 diversification within Pyrgomorphidae took place throughout the Cretaceous and well into the Cenozoic (Mariño- Pérez & Song, 2019). Currently, two subfamilies, Orthacridinae and Pyrgomorphinae, are recognized with 31 tribes, 148 genera, and 488 valid species (Cigliano et al., 2021). FIGURE 1. Diversity of Pyrgomorphidae. A. Psedna nana (Rehn, 1953) (Australia: Western Australia); B. Atractomorpha sp. (Papua New Guinea: New Britain); C. Monistria concinna (Walker, 1871) (Australia, NSW); D. Sphenarium histrio Gerstaecker, 1884 (Mexico, Oaxaca); E. Zonocerus elegans (Thunberg, 1815) (South Africa, KZN); F. Dictyophorus spumans (Thunberg, 1787) (South Africa: KZN). Photo credit: (A, B, C, E, F) Hojun Song; (D) Ricardo Mariño-Pérez. The current taxonomic classification of Pyrgomorphidae is mostly based on Kevan’s lifelong work (Kevan, 1952a, 1952b, 1963, 1966a, 1966b, 1968a, 1968b, 1969, 1970, 1982, 1990; Kevan & Akbar, 1964; Kevan et al., 1969, 1970, 1971, 1972, 1974; Kevan et al., 1975; Kevan & Chen, 1969; Kevan & Hsiung, 1985, 1989; Kevan et al., 1964). Kevan & Akbar (1964) provided a detailed account of the systematic history of the family, but expressed that it was difficult to subdivide the family into clear groups due to a high degree of morphological convergence and parallelism among different lineages as well as a large number of lineages that are uniquely distinct in terms of both external morphology and male phallic structures. A similar sentiment was expressed earlier by Dirsh (1961) who attempted to produce a preliminary classification of Acridomorpha. Nevertheless, Kevan and colleagues established two informal groups, ‘A’ and ‘B’ and recognized 31 tribes which were arranged into 10 series, with the Series I to IV belonging to the group ‘A’, and the Series V-X belonging to the group ‘B’ based on their extensive study of external morphology and male genitalia (Kevan & Akbar, 1964; Kevan et al., 1969, 1970, 1971, 1972, 1974; Kevan et al., 1975). Later, Otte (1994), in his synonymic catalogue of Orthoptera, elevated the informal groups ‘A’ and ‘B’ to the subfamily level and recognized Orthacridinae and Pyrgomorphinae, respectively, but provided no justification for this action. However, the taxonomic validity of these groupings, especially whether they represent monophyletic groups or not, has not been rigorously tested. While a number of modern phylogenetic studies on Orthoptera included various members of Pyrgomorphidae in a broader context (Fenn et al., 2008; Flook et al., 1999, 2000; Flook & Rowell, 1997; Rowell & Flook, 1998; Song et al., 2015), two recent studies have explicitly focused on resolving the phylogeny of this family. The first study was a cladistic analysis based on 28 out of 31 current recognized tribes and 119 morphological characters (Mariño-Pérez & Song, 2018). This work was the first explicit test of Kevan’s scheme (Kevan & Akbar, 1964; 102 · Zootaxa 4969 (1) © 2021 Magnolia Press ZAHID ET AL. Kevan et al., 1969, 1970, 1971, 1972, 1974; Kevan et al., 1975). It found the monophyly of the Group ‘A’ or the subfamily Orthacridinae, but found the Group ‘B’ or the subfamily Pyrgomorphinae as paraphyletic. For the 10 series, only the Series X (consisting of Pyrgomorphini and Chrotogonini) was found to be monophyletic, while the remaining series were paraphyletic. This study revealed that the currently accepted taxonomic classification for Pyrgomorphidae would require a comprehensive revision to accurately reflect the phylogeny. Instead of two subfamilies, Mariño-Pérez & Song (2018) recovered four monophyletic groups within Pyrgomorphidae, which were supported by different numbers of synapomorphies. However, the Bremer support values for these four clades were either 1 or 2, suggesting relatively weak support for these lineages. The second study was a molecular phylogeny of Pyrgomorphidae aiming at addressing the origin of the New World species (Mariño-Pérez & Song, 2019). This work used mitochondrial genomes and four nuclear genes and included 25 pyrgomorph species, including representatives of all four tribes present in the New World: Sphenariini, Ichthiacridini, Ichthyotettigini, and Omurini. This work robustly demonstrated that ancestral Pyrgomorphidae independently colonized the New World from the Old World at least three times. While testing Kevan’s scheme was not the aim of their study, the molecular phylogeny did result in a strikingly different topology than their earlier morphological phylogeny (Mariño-Pérez & Song, 2018) and failed to recover Orthacridinae as a monophyletic group. In discussing the discrepancies between the two studies, they attributed to the rampant morphological convergence within Pyrgomorphidae that could have caused confusion when coding morphological characters and states (Mariño-Pérez & Song, 2019). In this context, we aim to critically re-examine the utility of morphological characters originally used by Kevan and colleagues to establish the current classification scheme in light of a more expanded molecular phylogeny. Specifically, we test the monophyly of Kevan’s Groups ‘A’ and ‘B’ and the concept of Kevan’s series (Kevan & Akbar, 1964; Kevan et al., 1969, 1970, 1971, 1972, 1974; Kevan et al., 1975), as well as the monophyly of four clades recovered by Mariño-Pérez & Song (2018) using a molecular phylogenetic analysis based on mitochondrial genome, as well as the ancestral character state reconstruction analyses. We highlight the problem of the current taxonomic classification and suggest a possible direction to achieve a natural classification for

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