Trabajo Científico Article ISSN 0373-5680 (impresa), ISSN 1851-7471 (en línea) Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 Breaking the rule: multiple patterns of scaling of sexual size dimorphism with body size in orthopteroid insects BIDAU, Claudio J. 1, Alberto TAFFAREL2,3 & Elio R. CASTILLO2,3 1Paraná y Los Claveles, 3304 Garupá, Misiones, Argentina. E-mail: [email protected] 2,3Laboratorio de Genética Evolutiva. Instituto de Biología Subtropical (IBS) CONICET-Universi- dad Nacional de Misiones. Félix de Azara 1552, Piso 6°. CP3300. Posadas, Misiones Argentina. 2,3Comité Ejecutivo de Desarrollo e Innovación Tecnológica (CEDIT) Felix de Azara 1890, Piso 5º, Posadas, Misiones 3300, Argentina. Quebrando la regla: multiples patrones alométricos de dimorfismo sexual de tama- ño en insectos ortopteroides RESUMEN. El dimorfismo sexual de tamaño (SSD por sus siglas en inglés) es un fenómeno ampliamente distribuido en los animales y sin embargo, enigmático en cuanto a sus causas últimas y próximas y a las relaciones alométricas entre el SSD y el tamaño corporal (regla de Rensch). Analizamos el SSD a niveles intra- e interes- pecíficos en un número de especies y géneros representativos de los órdenes or- topteroides mayores: Orthoptera, Phasmatodea, Mantodea, Blattodea, Dermaptera, Isoptera, y Mantophasmatodea. La vasta mayoría de las especies mostraron SSD sesgado hacia las hembras, pero numerosas excepciones ocurren en cucarachas y dermápteros. La regla de Rensch y su inversa no constituyeron patrones comunes, tanto a nivel intraespecífico como interespecífico, con la mayoría de las especies y géneros mostrando una relación isométrica entre los tamaños de macho y hembra. En algunos casos, los patrones alométricos hallados podrían relacionarse con la va- riación geográfica del tamaño corporal. También demostramos que no todos los es- timadores de tamaño corporal producen el mismo grado de SSD y que el dimorfismo puede estar influenciado por un gran número de condiciones de vida y patrones de desarrollo ninfal. Finalmente, discutimos nuestros resultados en relación a modelos actuales de la evolución del dimorfismo sexual de tamaño en animales. PALABRAS CLAVE. Tamaño corporal. Blattodea. Dermaptera. Mantodea. Man- tophasmatodea. Caracteres morfométricos. Orthoptera. Phasmatodea. Regla de Rensch. Alometría. ABSTRACT. Sexual size dimorphism (SSD) although a widespread phenomenon among animals, is both enigmatic as to its proximate and ultimate causes and the scaling relationships between SSD and body size (Rensch’s rule). We analyzed SSD at the intra- and interspecific levels in a number of representative species and genera of the major orthopteroid orders: Orthoptera, Phasmatodea, Mantodea, Blat- todea, Dermaptera, Isoptera, and Mantophasmatodea. The vast majority of the spe- cies showed female biased SSD but numerous exceptions occur in cockroaches and earwigs. Rensch’s rule and its converse are not common patterns at both, intra- and cross-species level, most species and genera showing an isometric relation- ship between male and female body sizes. In some but not all cases, the demon- strated allometric patterns could be related to geographic body size variation. We also showed that not all body size estimators produce the same degree of SSD and that dimorphism can be strongly influenced by a number of living conditions and the patterns of nymphal development. Finally, we discuss our results in relation to Recibido: 14-I-2016; aceptado: 17-III-2016 11 Revista de la Sociedad Entomológica Argentina 75 (1-2): 11-36, 2016 current models of the evolution of sexual size dimorphism in animals. KEY WORDS. Body size. Blattodea. Dermaptera. Mantodea. Mantophasmatodea. Morphometric traits. Orthoptera. Phasmatodea. Rensch’s rule. Scaling. INTRODUCTION son, 1994; Fairbairn, 2013). SSD is a controversial aspect of evolutionary biology for several reasons. The length range of living systems is aston- On one side, although sexual selection has tradi- ishing: it spans 17 orders of magnitude from tionally been assumed as the key process behind DNA molecules to ecosystems; while organisms SSD, it is now well known that natural selection vary 7 orders of magnitude in length and 21 in can also produce size differences between males mass (Ellers, 2001). Insects have an impressive and females and that both processes are not com- body size range, from less than 0.2 mm in the pletely independent from one another (e.g. Isaac, parasitic wasp Dicopomorpha echmepterygis 2005; Carranza, 2009). This problem includes (Mymaridae) to ca. 360 mm in the stick-insect the study of the adaptive significance of SSD, the Phobaeticus chani (Phasmatidae). Body mass genetic constraints to its evolution, and its proxi- varies accordingly with females of the giant mate and ultimate causes (Fairbairn, 1997, 2007). weta, Deinacrida heteracantha (Anostostoma- Secondly, a problem which has not received a tidae) weighing more than 70 g (Björkman et satisfactory explanation is that of the allometric al., 2009). The enormous amount of scientific scaling of SSD with body size. Bernhard Rensch literature relative to animal body size reflects (1950, 1960) proposed that in phylogenetically re- the importance of this trait in biology. Almost lated species, SSD increases with general body every life history and ecological characteristic size when males are larger than females and of animals is correlated with body size (LaBar- decreases when females are larger. This pattern bera, 1986, 1989; Calder, 1996; Smith & Lyons, was termed Rensch´s rule by Abouheif & Fair- 2013) and in turn body size is strongly affected bairn (1997) but despite numerous studies in very by most ambient abiotic and biotic factors (Gas- diverse taxa (Fairbairn et al., 2007) there is little ton, 1991; Chown & Gaston, 2010, 2013; Price evidence to support this rule and no convincing et al., 2011). Thus, most physical, physiologi- mechanism for its operation has been proposed cal, ecological, and evolutionary processes are (Reiss, 1989; Webb & Freckleton, 2007; Bidau & highly dependent on size; these relationships Martí, 2008a; Martínez et al., 2014). are called scale effects or scaling. As defined Further problems regarding the scaling of by Barenblatt (2003), scaling “… describes a SSD with body size remain. In the first place, seemingly very simple situation: the existence there is the question of the taxonomic level at of a power-law relationship between certain which it is studied, and if Rensch’s rule operates variables y and x, y = Axα, where A, α are con- (if it does) in any taxonomic entity. Most studies stants.” This so-called allometric equation is of the scaling of SSD with body size either phylo- usually expressed in logarithmic form as log y = genetically-based or not have been performed log A + αlog x. The concept of allometric scal- across species at different levels (Fairbairn et ing was initially developed by Otto Snell (1892), al., 2007), and only a few intraspecifically as for D’Arcy Wentworth Thompson (1917), and Julian example, in insects, some grasshoppers and Huxley (1932) and resulted in numerous theo- beetles (e.g. Bidau & Martí, 2008b; Stillwell & retical and empirical investigations of the scal- Fox, 2009; Blanckenhorn et al., 2007a,b). An ing laws regulating the allometric relationship additional problem is that of the appropriate of many organismic traits with body size (e.g. measurements for analyzing SSD (Fairbairn, Schmidt-Nielsen, 1975, 1984; Brown & West, 2007). Is it the same using body mass or body 2005; Hoppeler & Weibel, 2005). length, or some other measurement (e.g. pro- Differences in body size between sexes (sexu- notum width, wing length) as a proxy for body al size dimorphism, SSD) are pervasive in the ani- size? Are SSDs for different measurements sig- mal kingdom and thus, a fundamental component nificantly correlated? (Martínez et al., 2014). of body size variation (e. g. Darwin, 1871; Anders- Orthopteroids do not only vary greatly in 12 BIDAU, C. J. et al. Sexual size dimorphism in orthopteroid insects size (Nasrecki, 2004; Bell et al., 2007; Whit- cliens (Stål) (6 populations, 56♂/58♀) (Table 1). man, 2008; Brock & Hasenpusch, 2009) but Most studies of geographic variation of body size also in the magnitude of SSD and in body of orthopteroids are based on different linear mea- shape (Hochkirch & Gröning, 2008; Bidau et surements. However, different authors use different al., 2013; Bidau, 2014). Furthermore, many estimators of body size. For example, body length species are fairly common, easy to collect, and and length of hind femur are commonly used mea- have large geographic distributions that allow surements but in some groups (e.g. Gryllidae and the sampling of several populations inhabiting Proscopiidae) researchers tend to favor measure- different or even contrasting environments (Bi- ments of the head and the pronotum as proxies for dau et al., 2012). The latter is relevant because body size. Body mass measurements are extreme- it has been suggested that in species showing ly rare in these insect groups thus, few cases of intraspecific geographic variation in body size body mass SSD were included in this study. Some (e.g. Bergmann’s rule [Bergmann, 1847]) there studies included only one measurement of body may exist a link between these patterns and the size while others, reported variation in male and scaling of SSD with body size (Blanckenhorn female size of up to 10-plus linear characters. The et al., 2006). In this sense orthopterans