Non-swarming grasshoppers exhibit density-dependent phenotypic plasticity reminiscent of swarming locusts

Highlights

• We quantified density-dependent phenotypic plasticity in two grasshopper species.

• Non-swarming Schistocerca species show density-dependent phenotypic plasticity.

• Both species change behavior, color, and morphology in response to crowding.

• There are similarities and differences in reaction norms between the two species.

• Our findings may be attributed to phylogenetic conservatism within the genus.

Abstract

Locusts are well known for exhibiting an extreme form of density-dependent phenotypic plasticity known as locust phase polyphenism. At low density, locust nymphs are cryptically colored and shy, but at high density they transform into conspicuously colored and gregarious individuals. Most of what we know about locust phase polyphenism come from the study of the desert locust Schistocerca gregaria (Forskål), which is a devastating pest species affecting many countries in North Africa and the Middle East. The desert locust belongs to the grasshopper genus Schistocerca Stål, which includes mostly non-swarming, sedentary species. Recent phylogenetic studies suggest that the desert locust is the earliest branching lineage within Schistocerca, which raises a possibility that the presence of density-dependent phenotypic plasticity may be a plesiomorphic trait for the whole genus. In order to test this idea, we have quantified the effect of rearing density in terms of the resulting behavior, color, and morphology in two non-swarming Schistocerca species native to Florida. When reared in both isolated and crowded conditions, the two non-swarming species, Schistocerca americana (Drury) and Schistocerca serialis cubense (Saussure) clearly exhibited plastic reaction norms in all traits measured, which were reminiscent of the desert locust. Specifically, we found that both species were more active and more attracted to each other when reared in a crowded condition than in isolation. They were mainly bright green in color when isolated, but developed strong black patterns and conspicuous background colors when crowded. We found a strong effect of rearing density in terms of size. There were also more mechanoreceptor hairs on the outer face of the hind femora in the crowded nymphs in both species. Although both species responded similarly, there were some clear species-specific differences in terms of color and behavior. Furthermore, we compare and contrast our findings with those on the desert locust and other relevant studies. We attribute the presence of density-dependent phenotypic plasticity in the non-swarming Schistocerca species to phylogenetic conservatism, but there may be a possible role of local adaptation in further shaping the ultimate expressions of plasticity.

Introduction

Density-dependent phenotypic plasticity is a defining feature of locusts (Pener and Simpson, 2009, Sword and Simpson, 2008). Locusts are grasshoppers that can form dense migrating swarms through a phenomenon known as locust phase polyphenism, in which cryptically colored, shy individuals (solitarious phase) can transform into conspicuously colored, gregarious individuals (gregarious phase) in response to increases in population density (Pener, 1983, Uvarov, 1966). In addition to color and behavioral changes, locusts exhibit morphological, reproductive, developmental, physiological, biochemical, molecular, and ecological changes in response to change in density (Applebaum et al., 1997, Hassanali et al., 2005, Kang et al., 2004, Pener, 1991, Pener and Simpson, 2009, Roessingh and Simpson, 1994, Simpson et al., 1999, Simpson et al., 2002, Simpson and Miller, 2007, Sword and Simpson, 2008, Tanaka, 2001, Tanaka, 2006, Verlinden et al., 2009). One of the most well studied examples is the desert locust, Schistocerca gregaria (Forskål), which is the biblical plague locust recorded in ancient literatures that still affects many lives in Africa and the Middle East (Pener and Simpson, 2009). The desert locust has been studied in depth since Uvarov (1928) showed the existence of locust phase, but over the last two decades, tremendous advances have been made in understanding proximate mechanisms of locust phase polyphenism and swarm formation (Pener and Simpson, 2009). We now know that behavioral gregarization of solitarious locusts can be induced by a combination of sight and smell of gregarious locusts (Despland, 2001, Hägele and Simpson, 2000, Roessingh et al., 1998) or by a physical stimulation of mechanosensory receptors located on the outer surface of hind femora (Simpson et al., 2001). These two sensory pathways transmit signals to the thoracic central nervous system (Rogers et al., 2003, Rogers et al., 2004), releasing serotonin [5-hydroxytryptamine (5-HT)], a conserved neuromodulator, which is shown to be responsible for the initial behavioral shift from the solitarious to gregarious phase (Anstey et al., 2009). A large number of phase-specific genes are expressed as a consequence (Badisco et al., 2011a, Badisco et al., 2011b), and at least one gene product cyclic Adenine Mono-Phosphate group (cAMP)-dependent protein kinase A (PKA), has been shown to play a critical role in initial behavioral gregarization (Ott et al., 2012). When scaled up to a population level, behavioral gregarization is a result of an interaction between local population increase and habitat structure (Bouaïchi et al., 1996, Collet et al., 1998, Despland, 2003, Despland et al., 2000). Once locusts are in the gregarious phase, they exhibit collective movement by aligning with other members of the group (Buhl et al., 2006) in the form of nymphal marching bands or adult swarms (Ellis, 1963, Kennedy, 1939, Uvarov, 1966). The resulting mass movement is partly driven by the risk of cannibalism (Bazazi et al., 2008).

The desert locust belongs to the genus Schistocerca Stål (Acrididae: Cyrtacanthacridinae), which contains about 50 species, widely distributed throughout the New World (Dirsh, 1974, Harvey, 1981, Song, 2004a). Within the genus, only four species are known to be swarming locusts (Harvey, 1981, Pener and Simpson, 2009, Song, 2011), and the majority of the species within Schistocerca are actually non-swarming, sedentary grasshoppers (Song, 2004b, Song, 2005, Song and Wenzel, 2008). Recent phylogenetic studies based on molecular data suggest that S. gregaria is the earliest branching lineage within the genus (Lovejoy et al., 2006, Song et al., 2013), which points to a possibility that the presence of density-dependent phenotypic plasticity may be an ancestral trait for the genus. However, little is known about the extent of density-dependent phenotypic plasticity in non-swarming species in the genus Schistocerca. Therefore it is of great interest to investigate whether non-swarming species in the genus are capable of expressing density-dependent phenotypic plasticity by experimentally varying rearing density during nymphal development. In this study, we examine two non-swarming Schistocerca species, Schistocerca americana (Drury) and Schistocerca serialis cubense (Saussure), both of which natively occur in Florida and are morphologically similar to the desert locust, but not known to swarm in nature (Harvey, 1981). Specifically, we address the following questions: (i) Do non-swarming Schistocerca species express density-dependent phenotypic plasticity in behavior, color, and morphology? (ii) How similar or different are the density-dependent plastic responses between the non-swarming species and the desert locust? and (iii) Are there species-specific differences in the plastic responses between the non-swarming species? The main motivation behind this study is to explicitly quantify density-dependent reaction norms in the non-swarming Schistocerca species with the same rigor as done in the desert locust in order to establish a comparative framework for studying the evolution of density-dependent phenotypic plasticity in Schistocerca.