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Diet, Bite Force and Skull Morphology in the Generalist Rodent Morphotype

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Diet, Bite Force and Skull Morphology in the Generalist Rodent Morphotype doi: 10.1111/jeb.12937 Diet, bite force and skull morphology in the generalist rodent morphotype R.MAESTRI*,B.D.PATTERSON†,R.FORNEL‡,L.R.MONTEIRO§ & T. R. O. DE FREITAS*¶ *Programa de Pos-Graduacßao~ em Ecologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil †Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA ‡Programa de Pos-Graduacßao~ em Ecologia, Universidade Regional Integrada do Alto Uruguai e das Miss~oes, Erechim, RS, Brazil §Laboratorio de Ci^encias Ambientais, CBB, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, RJ, Brazil ¶Departamento de Genetica, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil Keywords: Abstract chew; For many vertebrate species, bite force plays an important functional role. diet evolution; Ecological characteristics of a species’ niche, such as diet, are often associ- feeding; ated with bite force. Previous evidence suggests a biomechanical trade-off functional morphology; between rodents specialized for gnawing, which feed mainly on seeds, and gnaw; those specialized for chewing, which feed mainly on green vegetation. We myomorph; tested the hypothesis that gnawers are stronger biters than chewers. We natural selection; estimated bite force and measured skull and mandible shape and size in 63 phylogenetic path analysis; genera of a major rodent radiation (the myomorph sigmodontines). Analysis Rodentia; of the influence of diet on bite force and morphology was made in a com- sigmodontines. parative framework. We then used phylogenetic path analysis to uncover the most probable causal relationships linking diet and bite force. Both granivores (gnawers) and herbivores (chewers) have a similar high bite force, leading us to reject the initial hypothesis. Path analysis reveals that bite force is more likely influenced by diet than the reverse causality. The absence of a trade-off between herbivores and granivores may be associated with the generalist nature of the myomorph condition seen in sigmodontine rodents. Both gnawing and chewing sigmodontines exhibit similar, interme- diate phenotypes, at least compared to extreme gnawers (squirrels) and chewers (chinchillas). Only insectivorous rodents appear to be moving towards a different direction in the shape space, through some notable changes in morphology. In terms of diet, natural selection alters bite force through changes in size and shape, indicating that organisms adjust their bite force in tandem with changes in food items. aim of functional morphology (Wainwright, 1994). By Introduction studying ecologically relevant functions of organisms, Ecological morphology seeks to understand the associa- one can shed light on the relationships between ecol- tion between morphological variation and ecology in a ogy and function – it thus provides primary evidence of functional context (James, 1982). Understanding the adaptation. One such trait of obvious performance rele- mechanistic relationship between morphology and the vance and clear ecological function is bite force way it functions in the environment is thus a major (Aguirre et al., 2003; Herrel et al., 2005; Anderson et al., 2008; Santana et al., 2010). Bite force is an attribute related to numerous types of Correspondence: Renan Maestri, Programa de Pos-Graduac ßao~ em functional demands in vertebrates (e.g. feeding, mating, Ecologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS defence, competition) and may reflect the strength of 91501-970, Brazil. ecological challenges that organisms face (Anderson Tel.: +55(51)33087623; fax: +55(51)33087626; e-mail: [email protected] et al., 2008). Demands related to feeding are usually the ª 2016 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY. J. EVOL. BIOL. 29 (2016) 2191–2204 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2016 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 2191 2192 R. MAESTRI ET AL. primary selective agents determining bite force (Chris- Living rodents were traditionally divided into three tiansen & Wroe, 2007; Nogueira et al., 2009), although morphotypes based on masseter muscle configurations: intra- and interspecific competitive interactions can also sciuromorph, hystricomorph and myomorph (Brandt, play a role (Herrel et al., 2007; Anderson et al., 2008; 1855; Simpson, 1945). These three groups are no Cornette et al., 2015). Bite force is also known to be longer considered to be monophyletic (Wood, 1965; highly correlated with body size in vertebrates (Wroe Blanga-Kanfi et al., 2009; Fabre et al., 2012), although et al., 2005; Freeman & Lemen, 2008), although excep- they still reflect important and well-defined differences tions to this rule are most interesting. Skull shape, in skull and mandible morphology (Cox et al., 2012). which configures the position and arrangement of mus- The sciuromorph condition is characterized by a large cle masses and lever arms, may similarly play a role in masseter lateralis muscle that extends onto the rostrum, influencing bite force (Herrel et al., 2001; Nogueira and associated changes in the mandible’s angular pro- et al., 2009; Cornette et al., 2015; Wittorski et al., 2016). cess (Wood, 1965; Korth, 1994). These changes amplify Studies relating bite force with ecological functions the gnawing abilities of sciuromorph rodents (Druzin- have been extensively investigated in lizards (Herrel sky, 2010; Cox et al., 2012), giving them stronger bites et al., 2001; Wittorski et al., 2016), turtles (Herrel et al., than other rodents. On the other hand, the hystrico- 2002), birds (Herrel et al., 2005) and in several mam- morph condition represents a specialization for chew- mal orders (Wroe et al., 2005; Nogueira et al., 2009; ing. Morphological specialization involves the Cornette et al., 2015), including rodents (Van Daele enlargement of the masseter medialis, which passes et al., 2009; Willians et al., 2009; Blanco et al., 2012; through the infraorbital foramen (greatly enlarging it) Cox et al., 2012, 2013, 2015; Becerra et al., 2014; and inserts onto the rostrum (Wood, 1965; Korth, Druzinsky, 2015; Vassallo et al., 2015). However, inves- 1994). This condition allows rodents to be more effec- tigations of bite force in rodents have been limited to tive at feeding with the molars (Hautier et al., 2011; one or a few species, so that comparative assessments Cox et al., 2012). Hystricomorph rodents feed mainly using large data sets are still lacking. on vegetation, and most strictly herbivorous rodents The order Rodentia is considered the most success- have this morphotype; on the other hand, sciuromor- ful group in the 210-Ma history of mammals (Mered- phous rodents feed mainly on seeds and nuts and are ith et al., 2011). More than 40% of living mammal therefore granivorous. species are rodents (Wilson & Reeder, 2005; IUCN, Finally, rats and mice – members of the highly suc- 2016), and they occupy nearly all terrestrial ecosys- cessful Muroidea, which account for more than half of tems. Although their species richness exceeds that of all rodent species – are characterized by the myomor- other mammalian orders, their morphological varia- phous condition. This condition involves shifts and tion is thought to be relatively conserved (Hautier extensions of both masseter medialis and lateralis, effec- et al., 2011). Disparity in diet among living species tively combining features of both the sciuromorph and may result from changes in size and shape (Samuels, hystricomorph conditions (Wood, 1965; Korth, 1994). 2009), as well as in bite force (Hautier et al., 2011, Myomorphy is thought to represent a compromise 2012; Cox et al., 2012, 2013). between gnawing and chewing specializations, produc- Rodents are specialized towards a peculiar form of ing a generalist ‘jack-of-all-trades’ phenotype that has mastication, resulting in a characteristic skull that has a proven to be very successful. pair of ever-growing teeth, elongated rostrum and large Here, we explore the relationship between diet, bite masseter muscles (Wood, 1965; Korth, 1994). All force, skull and mandible morphology in one of the rodent species have a single incisor on each side of the world’s most explosive radiations (Schenk et al., 2013). jaw that is separated from the cheekteeth by a dia- Sigmodontines comprise a Neotropical subfamily of the stema. Occlusion of the incisors (for gnawing) and of muroid family Cricetidae and hence share the myomor- the cheekteeth (for grinding and chewing) take place in phous condition. Most of these rats and mice have gen- alternation, so that when the incisors are engaged, the eralist, omnivorous diets, feeding on fruits, seeds and cheekteeth do not contact each other and vice versa. insects in different proportions (Nowak, 1999; Patton This fundamental characteristic of rodents sets the stage et al., 2015). However, others have more specialized for an interesting trade-off between rodents specialized diets, such as the insectivorous and carnivorous mem- in gnawing (incisor engaged) or in chewing (cheekteeth bers of the tribe Ichthyomyini or the obligately herbivo- engaged; Cox et al., 2012), which is accompanied by rous rats of the genera Andinomys and Chinchillula changes in morphology. Rodents that use mostly the (Patton et al., 2015). Given the established relationships incisors (gnawers) are expected to have stronger bite among morphotypes and diet in rodents, here we ask forces at the incisor, and these rodents are prone to whether these patterns hold true for this radiation of feed on seeds and nuts; conversely, rodents that
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