On the origin of the New World Pyrgomorphidae (Insecta: Orthoptera)
Graphical abstract
Introduction
Pyrgomorphidae (Orthoptera: Caelifera) are one of the most charismatic grasshopper families, well known for their vibrant body color and conspicuous sculpting patterns on pronotum, often featured in display collections of large and showy insects (Mariño-Pérez and Song, 2018). The family currently includes 487 valid species, most of which occur in the Old World, with a great majority (384 species) distributed in Africa and Asia. While some of the most colorful members of the family are familiar to the general public and well studied, the majority of pyrgomorphs are actually cryptic and less known. Among these insects, perhaps the least studied species are the assemblages of pyrgomorphs that have diversified in the New World.
In the New World, there are only 41 species of Pyrgomorphidae (8.4% of total diversity in the family), representing 13 genera (Kevan and Akbar, 1964). The New World Pyrgomorphidae (NWP) consist of four tribes and show very specific distribution patterns. Ichthiacridini (3 genera; 10 spp.) and Ichthyotettigini (4 genera; 7 species) are both endemic to Mexico, and Omurini (3 genera; 4 spp.) is found in the northern half of South America. The tribe Sphenariini includes four subtribes, of which only one subtribe (Sphenariina; 3 genera; 20 spp.) is found in the New World, distributed from Mexico to Costa Rica and Dominican Republic (Cigliano et al., 2019). The remaining three subtribes of Sphenariini are disjunctly distributed in Madagascar, East Africa, and China, respectively. Because most pyrgomorphs are found in the Old World, the presence of these insects in the New World has drawn attention of several taxonomists. There have been three main biogeographical hypotheses proposed to explain the origin and diversification of the NWP. The first one was by Kevan and Akbar (1964) who hypothesized that the ancestral pyrgomorphs could have colonized the Americas at least twice from Asia. They based their hypothesis on the strong morphological resemblance (in body form and male internal genitalia) between the Chinese genera Yunnanites Uvarov and Mekongiana Uvarov (Sphenariini: Mekongianina) and the Mexican genus Sphenarium (Sphenariini: Sphenariina), and between the Asian members of the tribe Orthacridini and the Mexican tribes and Ichthiacridini and Ichthyotettigini. Kevan (1978) recognized that the family represents an ancient lineage and even invoked “Lemuria”, a hypothetical and now discredited land bridge that was thought to exist in the Pacific to explain the distribution of pyrgomorphs in the Pacific islands. However, he thought that the NWP resulted from multiple colonization events from the ancient pyrgomorphs that originated from Asia, crossed the Bering land bridge to arrive in the New World and ultimately reach Central and South America. The second hypothesis was made by Amédégnato (1993) who considered Pyrgomorphidae to be closely related to the Old World grasshopper families, Pamphagidae and Lentulidae, as well as the South American endemic Tristiridae based on their male genitalia. She thought that Pyrgomorphidae originated in Asia and dispersed to Africa and some lineages colonized South America when the two continents were physically close. However, she did not specify how many times the colonization of South America could have taken place. The hypotheses of Kevan and Amédégnato have not been formally tested in a phylogenetic framework. The third hypothesis was proposed by Mariño-Pérez and Song (2018), who conducted the first modern cladistic analysis of Pyrgomorphidae based on morphology. They found that the NWP did not form a monophyletic group based on a morphological phylogeny, suggesting that the New World has been colonized by ancestral pyrgomorphs from the Old World multiple times, but due to the scope of the paper, the exact origin in the Old World was not hypothesized. Unfortunately, none of the three biogeographical hypotheses has taken into account any time component.
Morphologically, the NWP are characterized by their body forms that generally fall in two categories: fusiform, in which the head is conical, the pronotum expands towards metazona and the abdomen stretches towards its end. The second form is cylindrical, in which the body has the same width throughout the entire body (Fig. 1). Regarding wings, there is a large variation from having fully functional wings (macropterous as in Minorissa Walker) to very reduced non-functional wings (micropterous as in Sphenarium Charpentier) and to complete loss of wings (apterous as in Ichthyotettix Rehn) (Mariño-Pérez and Song, 2018). Ecologically, the NWP occupy diverse habitats from sea level up to 2700 masl. They can be found in deciduous or semideciduous tropical forest, rainforest, cloud forest, pine forest, grasslands, xeric scrub and thorny scrub. They prefer open spaces with sunlight, usually found on the ground or perching on grasses, shrubs, trees and cacti (see Table 1). Of the NWP, the genus Sphenarium has been studied in depth in terms of their mating biology (Cueva del Castillo, 2003, Cueva del Castillo and Núñez-Farfán, 1999), variation in size and color (Alves Dos Santos, 2005, Sanabria-Urbán et al., 2015, Sanabria-Urban et al., 2017), and phylogeographic patterns (Sanabria-Urbán et al., 2015, Sanabria-Urban et al., 2017). For example, Sphenarium species show some of the longest mate guarding behavior in which males can spend up to 22days (half of its adult life) after copulation mounted on the females (Cueva del Castillo, 2003, Cueva del Castillo and Núñez-Farfán, 1999). In some areas in Mexico, Sphenarium species are agriculturally important pests of crops such as corn and beans (COPR, 1982), while in Oaxaca they have been used as food (known as chapulines) for centuries (Cerritos and Cano-Santana, 2008).
In this study, we have investigated the biogeography of the NWP based on a molecular phylogeny generated using complete mitochondrial genomes and four nuclear genes. We have included representatives of all four lineages known from the New World, as well as a number of the Old World representatives of the family. We specifically test the three biogeographical hypotheses regarding the origin of the NWP, and infer a biogeographical scenario based on a divergent time estimate and a biogeographical analysis. We show that the current distribution of the NWP is a result of dynamic vicariance and dispersal events and propose a novel biogeographical hypothesis regarding the origin and diversification of the NWP.
Section snippets
Taxon and character sampling
We sampled a total of 32 taxa, including 7 outgroup taxa representing 7 families of Acridomorpha (Acrididae, Lentulidae, Pyrgacrididae, Pamphagidae, Pneumoridae, Trigonopterygidae, and Tanaoceridae) and 25 ingroup taxa representing the Pyrgomorphidae. Particularly, we included representatives of all four tribes present in the New World: Sphenariini, Ichthiacridini, Ichthyotettigini, and Omurini. For all terminals, we included partial or complete mitochondrial genome (mtgenome) data, 21 of which
Phylogeny of Pyrgomorphidae and the position of the New World genera
We recovered monophyletic Pyrgomorphidae with strong nodal support in both ML and Bayesian analyses (Fig. 2). The tree tropology was highly congruent between the two analyses and only three taxa with low support value in the ML analysis (Atractomorpha sinensis, Mekongiella kingdoni and Chrotogonus sp.) were incongruent in both topologies but their placements did not affect our discussion and conclusion about the origin of the NWP. The NWP did not form a monophyletic group, but instead resulted
Phylogeny of Pyrgomorphidae and the placement of the New World genera
This study represents the first formal test of the monophyly of New World Pyrgomorphidae based on molecular data. Previous molecular studies included some members of Pyrgomorphidae as part of their taxon sampling, but did not specifically set out to understand the internal relationships of this family. For example, Flook and Rowell (1997) included three Pyrgomorphidae taxa (Prosphena scudderi, Atractomorpha acutipennis and Zonocerus elegans), Flook et al., 1999, Flook et al., 2000 included
Conclusions and future directions
Despite the low number of species of Pyrgomorphidae in the New World, its origin is very old and complex. We have provided evidence and rationale about the biogeography of the NWP based on a molecular phylogeny. We infer that the first wave of colonization was probably due to a vicariance event (split of Africa and South America) or dispersal from West Africa to northern South America with a subsequent dispersal from South America to the Caribbean. It is probable that the first fauna of NWP was
Declaration of Competing Interest
Author declares that there is no conflict of interest.
Acknowledgements
We thank Antoine Foucart, Gavin Svenson, Salomón Sanabria-Urbán, and Michael Whiting for collecting and providing specimens, and Joey Mugleston, Jorge Humberto Medina-Durán and Steve Gotham for providing assistance in collecting in the field. We would also like to thank Brigido Hierro and Daniel Perez-Gelabert for their help during our trip to Dominican Republic to collect Jaragua under authorization number 1424 and export permit number 692. Fieldwork to South Africa and Australia was conducted
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