Phylogeny of bird-grasshopper subfamily Cyrtacanthacridinae (Orthoptera: Acrididae) and the evolution of locust phase polyphenism

Locust phase polyphenism is an extreme form of density-dependent phenotypic plasticity in which solitary and cryptic grasshoppers can transform into gregarious and conspicuous locusts in response to an increase in local population density. We investigated the evolution of this complex phenotypic plasticity in a phylogenetic framework using a morphological phylogeny of Cyrtacanthacridinae, which contains some of the most important locust species, and a comprehensive literature review on the biology and ecology of all known members of the subfamily. A phylogenetic analysis based on 71 morphological characters yielded a well-resolved tree and found that locust phase polyphenism evolved multiple times within the subfamily. The literature review demonstrated that many cyrtacanthacridine species, both locust and sedentary, are capable of expressing density-dependent color plasticity. When this color plasticity was divided into two smaller components, background coloration and development of black pigmentation, and when these plastic traits were optimized on to the phylogeny, we found that the physiological mechanisms underlying this plasticity were plesiomorphic for the subfamily. We also found that different locust species in Cyrtacanthacridinae express both similarities and differences in their locust phase polyphenism. Because locust phase polyphenism is a complex syndrome consisting of numerous plastic traits, we treat it as a composite character and dissected it into smaller components. The similarities among locust species could be attributed to shared ancestry and the differences could be attributed to the certain components of locust phase polyphenism evolving at different rates. The Willi Hennig Society 2007. Phenotypic plasticity is the ability of a genotype to produce different phenotypes in response to different environmental conditions (Schlichting and Pigliucci, 1998). How organisms respond and interact with their environment and the evolutionary consequences of this interaction have become one of the most important subjects in evolutionary biology (Pigliucci, 2001). Evolutionary biologists have studied the evolution of phenotypic plasticity from various biological contexts from experimental biology, developmental biology and theoretical biology to quantitative genetics (Pigliucci, 2001; Schlichting and Smith, 2002; West-Eberhard, 2003; Pigliucci, 2005). One area of biology that is distinctly missing from the study of phenotypic plasticity is the historical perspective (Doughty, 1995; Pigliucci et al., 1999; Kembel and Cahill, 2005). Phenotypic plasticity is usually investigated at the level of individuals and populations and rarely addressed in a comparative framework. Perhaps this may be because researchers are mostly interested in understanding adaptive plasticity, which can be best studied at microevolutionary scale (Schlichting and Pigliucci, 1998; West-Eberhard, 2003). Because phenotypic plasticity is often considered to have evolved as an adaptation to heterogeneous environment (but see Sword, 2002), the focus has been on studying the interaction between a species and its current environment, rather than studying the evolutionary history of the origin and expression of phenotypic plasticity. Another reason for the lack of *Corresponding author: E-mail address: [email protected] Present address: Department of Integrative Biology, Brigham Young University, Provo, UT 84602, USA. The Willi Hennig Society 2007 Cladistics 10.1111/j.1096-0031.2007.00190.x Cladistics 23 (2007) 1–28 historical perspective may simply be the difficulty of obtaining necessary experimental data from a phenotypically plastic species and its close relatives. For example, a particular plant species is experimentally demonstrated to express plasticity in developmental rate in response to day length (as in Arabidopsis thaliana, Mozley and Thomas, 1995), but this does not necessarily mean that its sister species expresses the same plasticity; it has to be shown experimentally in the same environmental condition. The more species the clade of interest contains, the more difficult the task becomes. However, studying the evolution of phenotypic plasticity from an historical context can provide invaluable insight regarding the phenomena we observe today (Doughty, 1995). If two species in a clade express a type of phenotypic plasticity to a certain environmental cue and if they are shown to be sister species in a robust phylogeny, their ability to express plastic phenotypes can be attributed to common ancestry, rather than adaptation. This idea is comparable with understanding of the evolution of ecological characters from a phylogenetic framework (Brooks and McLennan, 1991; Harvey and Pagel, 1991; Miller and Wenzel, 1995). This has an important consequence in terms of studying the evolution of plasticity. Typically, a null hypothesis in the study of phenotypic plasticity in a particular species is a zero slope reaction norm (Doughty, 1995). For instance, in order to show that a species has phenotypic plasticity, one need only reject the null hypothesis that the reaction norm of this species has a zero slope. However, if this species belongs to a clade whose members express phenotypic plasticity, the null hypothesis would be a non-zero slope. Then, one must show the differences in slope to reject the null hypothesis and conclude that evolution shaped or changed the reaction norm in question. Therefore, understanding phylogeny can provide a more accurate starting point in studying the evolution of phenotypic plasticity. Locusts are excellent candidates to address the interaction between phylogeny and phenotypic plasticity. Locusts are grasshoppers belonging to Acrididae (Orthoptera) that can form dense migrating swarms through a phenomenon known as locust phase polyphenism (Pener, 1983). Because they are defined by phenotypic plasticity, locusts are not a taxonomic group and there are at least 15 known locust species belonging to six acridid subfamilies (Song, 2005). Typically, these insects are cryptically colored, solitary individuals at low density (called the ‘‘solitarious phase’’; Fig. 1), but when environmental conditions lead to increase in population density, they transform into conspicuously colored, gregarious individuals (called the ‘‘gregarious phase’’; Fig. 1) (Uvarov, 1966; Pener, 1991; Pener and Yerushalmi, 1998). In addition to color and behavior, morphology, endocrine action, biochemistry, nutritional intake, and genetic expression also change in response to change in density (Simpson et al., 1999, 2002; Breuer et al., 2003; Tawfik and Sehnal, 2003; Kang et al., 2004; Hassanali et al., 2005). When the high-density condition persists, the population size increases rapidly, which leads to the formation of dense migrating groups known as a locust swarm. Locust phase polyphenism can thus be considered an extreme form of density-dependent phenotypic plasticity. Different components of locust phase polyphenism are, however, not always tightly linked and it is possible to find individuals with conspicuous coloration or constricted pronotum without gregarious behavior (Uvarov, 1966), although these traits are often expressed together. The exact function of color plasticity in Cyrtacanthacridinae is not clear, but recent studies have suggested that it could be adaptive density-dependent aposematism (Sword, 1999, 2002; Sword et al., 2000). In short, when nymphs live in a low-density condition, they benefit from having a cryptic coloration. But when the population density increases, they will actively feed on toxic plants, which coincides with the expression of conspicuous coloration (Sword, 1999). Vertebrate predators have been shown to quickly associate this conspicuous coloration with toxicity (Sword, 1999; Sword et al., 2000). Migratory band formation can also be adaptive in that it can function as an antipredator strategy in conjunction with aposematism (Simpson et al., 2005). In this study, we investigate the evolution of locust phase polyphenism from an historical context using a phylogeny of the bird-locust subfamily Cyrtacanthacridinae (Orthoptera: Acrididae) based on morphological characters. Most species in the subfamily are sedentary and do not form swarm (Uvarov, 1923), but the subfamily contains some of the most important locust Fig. 1. Last instar nymphs of gregarious (left) and solitarious (right) phase of a locust species, Schistocerca piceifrons. In a low population density, locust nymphs are cryptic green and avoid other individuals. When a population density increases, they transform into conspicuous and highly aggregating individuals. 2 H. Song and J. W. Wenzel / Cladistics 23 (2007) 1–28