On the origin of the New World Pyrgomorphidae (Insecta: Orthoptera)

Highlights

• The molecular phylogeny of the New World Pyrgomorphidae was reconstructed for the first time.

• Pyrgomorphidae is recovered as monophyletic.

• New World Pyrgomorphidae are not monophyletic.

• New World Pyrgomorphidae are results of two independent colonizations from Africa, around 96 and 69 mya.

Abstract

The gaudy grasshopper family Pyrgomorphidae (Orthoptera: Caelifera) shows a peculiar geographical distribution. Of the 487 described species, less than 10% of the diversity is found in the New World, while the rest occur throughout Africa, Asia, and Australia. Only 41 species belonging to four tribes are found in Central and South America and Dominican Republic, and the phylogenetic positions of these taxa within the large phylogeny of Pyrgomorphidae and the relationships among them have never been investigated. Regarding the biogeography, three different hypotheses about the origin of the New World Pyrgomorphidae have been proposed, but these have not been empirically tested. In this study, we present the first molecular phylogeny of Pyrgomorphidae that includes the members of all four New World tribes and representative genera from the Old World based on entire mitochondrial genome and four nuclear genes to investigate the biogeography of this fascinating lineage. Our results recover Pyrgomorphidae as monophyletic and the New World Pyrgomorphidae as a paraphyletic group comprising three clades, consisting of: (1) The Caribbean Jaragua + the South American Algete; (2) The Mexican and Central American Sphenarium + Prosphena; and (3) The Mexican lineages Ichthiacridini + Ichthyotettigini. The divergence time estimation analysis suggested that the Pyrgomorphidae diverged from its relatives in the Early Cretaceous (139–104 mya). The biogeographic analysis using BioGeoBEARS showed that after diversifying in the Old World, the first New World Pyrgomorphidae clade (Algete + Jaragua) diverged 96 mya (Late Cretaceous, Cenomanian) and that their current distribution in the New World is explained by two possible events, a transatlantic colonization from Africa to Northern South America or a vicariance event between these two landmasses, followed by a subsequent dispersal to the Caribbean. The second wave of colonization occurred about 69 mya towards the end of the Late Cretaceous (Maastrichtian) with dispersal from Africa to South America and then to North America with a subsequent diversification in Mexico including Baja California.

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.