Elsevier

Zoology

Volume 124, October 2017, Pages 61-72
Zoology

Ontogenetic and functional modularity in the rodent mandible

https://doi.org/10.1016/j.zool.2017.05.009Get rights and content

Highlights

  • Bony responses to diet within the mandible vary by region and by ontogenetic stage.

  • Morphogenesis is driven by tooth growth in the corpus, diet in the ramus.

  • The morphology of the coronoid–temporalis module reflects early weanling diet.

  • The angular–pterygomasseteric module has a longer plasticity window.

  • Morphology of the ramus in adults most strongly reflects diet and feeding history.

Abstract

The material properties of diets consumed by juvenile individuals are known to affect adult morphological outcomes. However, much of the current experimental knowledge regarding dietary effects on masticatory form is derived from studies in which individuals are fed a non-variable diet for the duration of their postweaning growth period. Thus, it remains unclear how intra-individual variation in diet, due to ontogenetic variation in feeding behaviors or seasonal resource fluctuations, affects the resulting adult morphology. Furthermore, the mandible is composed of multiple developmental and functional subunits, and the extent to which growth and plasticity among these modules is correlated may be misestimated by studies that examine non-variable masticatory function in adults only. To address these gaps in our current knowledge, this study raised Sprague Dawley rats (n = 42) in four dietary cohorts from weaning to skeletal maturity. Two cohorts were fed a stable (“annual”) diet of either solid or powdered pellets. The other two cohorts were fed a variable (“seasonal”) diet consisting of solid/powdered pellets for the first half of the study, followed by a shift to the opposite diet. Results of longitudinal morphometric analyses indicate that variation in the mandibular corpus is more prominent at immature ontogenetic stages, likely due to processes of dental eruption and the growth of tooth roots. Furthermore, adult morphology is influenced by both masticatory function and the ontogenetic timing of this function, e.g., the consumption of a mechanically resistant diet. The morphology of the coronoid process was found to separate cohorts on the basis of their early weanling diet, suggesting that the coronoid process/temporalis muscle module may have an early plasticity window related to high growth rates during this life stage. Conversely, the morphology of the angular process was found to be influenced by the consumption of a mechanically resistant diet at any point during the growth period, but with a tendency to reflect the most recent diet. The prolonged plasticity window of the angular process/pterygomasseteric muscle module may be related to delayed ossification and muscular maturation within this module. The research presented here highlights the importance of more naturalistic models of mammalian feeding, and underscores the need for a better understanding of the processes of both morphological and behavioral maturation that follow weaning.

Introduction

The fundamental goal of functional morphology is to understand the diversity of morphological forms in light of their environmental and behavioral roles. In recent years, phenotypic plasticity has been highlighted in the biological sciences for its potential to shed light on these form–function relationships. Phenotypic plasticity refers to the ontogenetic modulation of a phenotype across an environmental gradient (Stearns, 1989, West-Eberhard, 1993, West-Eberhard, 2005) and can function as a mechanism for the fine-tuning of form–function relationships across an individual’s lifespan (Grant and Grant, 1989, Galis, 1996).

Functional morphologists have long utilized the phenomenon of phenotypic plasticity to explore the link between diet and masticatory form in an experimental setting. By altering diet or even the masticatory apparatus itself, researchers have induced plastic responses through the process of skeletal functional adaptation (sensu Lanyon and Rubin, 1985) and stimulated the development of multiple functional phenotypes within a single laboratory species. These studies, in synthesis with inter-specific comparative work, have demonstrated that the basic principles of functional adaptation of the masticatory system are remarkably similar across mammalian taxa. The material properties of food items are understood to influence jaw adductor activity, jaw kinematics, and feeding behaviors (Crompton, 1986, Weijs et al., 1989; Hylander et al., 1992, Hylander et al., 2000, Hylander et al., 2005). Increased jaw muscle activity associated with mechanically resistant food items results in elevated peak and cyclical strains in the craniomandibular skeleton (Weijs and de Jongh, 1977, Hylander, 1979, Hylander, 1988, Hylander, 1992, Hylander et al., 1992, Herring and Teng, 2000, Ravosa et al., 2007, Ravosa et al., 2008b, Ravosa et al., 2015) and, in turn, differential growth and remodeling of hard and soft tissues in the cranium and mandible (Beecher and Corruccini, 1981, Bouvier and Hylander, 1981, Bouvier and Hylander, 1996, Beecher et al., 1983, Bouvier and Zimny, 1987, Bouvier, 1988, Yamada and Kimmel, 1991, Kiliaridis et al., 1996, Nicholson et al., 2006; Ravosa et al., 2007, Ravosa et al., 2008b, Ravosa et al., 2010, Menegaz et al., 2009, Menegaz et al., 2010, Scott et al., 2014a, Franks et al., 2016, Franks et al., 2017, Ravosa et al., 2016).

A common operating condition among most plasticity studies is that the function of interest is held static. For example, studies which experimentally manipulate dietary consistency often rely on a short- or long-term exposure to a stable, homogenous post-weaning diet (Beecher et al., 1983, Kiliaridis et al., 1996, Ravosa et al., 2008a, Menegaz et al., 2009, Menegaz et al., 2010, Ravosa et al., 2016). These homogenous diets do not necessarily reflect the natural variation in diet that occurs due to ontogenetic changes in feeding behaviors (Herring and Wineski, 1986, Hurov et al., 1988, Dardaillon, 1989, Janson and van Schaik, 1993, Bowler and Bodmer, 2011) or to fluctuations in resource availability (Robinson and Wilson, 1998, Marshall and Wrangham, 2007), yet such aspects of dietary variability may exert strong selective pressures on feeding morphology. A select number of studies of joint mechanobiology in rodents have addressed intra-individual variation in dietary composition and found that the masticatory complex of growing individuals may be capable of significant morphological plasticity in response to these dietary changes (Bouvier and Hylander, 1984, Bouvier and Zimny, 1987, Yamada and Kimmel, 1991). Furthermore, adaptive plasticity during early life stages, when growth rates are high, is thought to have an additive influence on underlying growth allometries (Bernays, 1986). In such cases, adult morphology would be strongly affected by the environmental conditions experienced during early life, and modified to a lesser degree by changes in habitat and diet experienced near or after skeletal maturity. Thus, the nature of phenotypic plasticity in the masticatory apparatus has important ramifications for feeding function and performance in mammalian taxa that experience ontogenetic changes in feeding behavior and/or inhabit variable environments.

Moreover, in holding function static in these experiments, we not only underestimate behavioral complexity but skeletal complexity as well. The skeletal morphology of the masticatory apparatus is the product of interactions between genetics, development, and multiple functional pressures (Atchley et al., 1992, Atchley, 1993). Even within a single skeletal element such as the mandible, multiple functional subunits (“modules”) exist that all interact uniquely with their associated soft tissues (Moss and Meehan, 1970, Klingenberg et al., 2003a, Zelditch et al., 2008). As feeding behavior changes over an individual’s life time (through suckling, weaning, and tooth eruption/replacement to the eventual achievement of skeletal maturity), so should the relative importance of functional demands placed on these various morphological modules. The ability of an organism to respond to the environment by means of morphological plasticity may decrease as growth and the rates of bone modeling slow (Hinton and McNamara, 1984, Bertram and Swartz, 1991, Rubin et al., 1992, Pearson and Lieberman, 2004, Hoverman and Relyea, 2007; but see Scott et al., 2014b). However, it is underappreciated to what extent the onset and rate of this decline in plasticity varies among the modules of the masticatory apparatus.

Indeed, the extent to which the growth of various morphological components within the mandible is correlated was addressed previously by Atchley et al. (1992). The authors tested multiple hypotheses of morphogenesis to explain variation in mandibular form between the two main genera of laboratory rodent (Mus and Rattus). Of these hypotheses, two models were considered that potentially explain the differential growth of the mandibular regions in these taxa. The muscle hypertrophy model posits that muscle–bone interactions occurring in the mandibular ramus could drive morphological variation, while the tooth growth model suggests that variation is related to interactions between the teeth and the mandibular corpus. Atchley et al. (1992) found in their study of adult rodents support for all hypotheses except the tooth growth model.

With the muscle hypertrophy and tooth growth models in mind, the present study evaluates the functional sources and the spatial distribution of variation in mandibular morphology at multiple ontogenetic stages within the lifespan of a single species (Rattus norvegicus). The goals of this research were two-fold. The first goal was to investigate the role of intra-individual variation in diet on mandibular morphology. We predicted that feeding behaviors during early, post-weaning life stages would have a disproportionate effect on morphological outcomes in adults due to ontogenetic decline in growth rates. The second goal was to explore longitudinal variation in phenotypic plasticity within the mandible. We predicted that the timing and rates of plasticity responses would vary among mandibular modules, with those modules related to masticatory function (e.g., joint and muscle attachment structures) showing the greatest response during periods in which the individual consumed a more mechanically resistant diet.

Accordingly, the present study attempted to model the temporal complexity of the material properties of mammalian diets in a laboratory setting. In addition to two treatment groups representing the static homogenous (“annual”) diets found in many previous studies, this work also included two variable diet cohorts that experienced a shift in dietary composition during their post-weaning growth period. An “early seasonal” cohort was weaned onto a non-mechanically challenging diet consisting of powdered meal, then switched to a more challenging diet consisting of solid compressed pellets at the mid-juvenile stage. This strategy models the weaning behavior of many mammalian species, which preferentially wean their young during periods of high availability for food items that are easily consumed by young individuals with deciduous or incomplete dentition and a still-growing musculoskeletal masticatory apparatus (Russell, 1984, Di Bitetti and Janson, 2000, Pride, 2005, Eckardt and Fletcher, 2013). As a comparison to the “early seasonal” cohort, a “late seasonal” cohort was weaned onto the challenging diet (compressed pellets), and then switched to the non-challenging diet (powdered meal) at the mid-juvenile stage.

Though the present study encompasses only a single shift in dietary properties, rather than repetitive shifts such as individuals in seasonally variable environments might experience over a longer lifespan, it represents an opportunity to examine how a marked change in dietary composition affects skeletal growth during the important period of growth between weaning and maturity. Additionally, this model accounts only for variation in dietary material properties, and not for the variation in nutritional content that also characterizes many seasonal diets (Conklin-Brittain et al., 1998, Marshall and Wrangham, 2007) and may influence craniomandibular growth (Miller and German, 1999, Fujita et al., 2016). Finally, the present study uses a longitudinal approach to better elucidate the relationship between diet and mandibular morphology across a single individual’s lifetime.

Section snippets

Experimental sample

All procedures for this project were conducted in accordance with an IACUC-approved protocol. A total of 42 male Sprague Dawley rats (Rattus norvegicus, RRID:RGD_5508397) (Berkenhout, 1769) were obtained from Harlan Laboratories (Haslett, MI, USA) as weanlings (22 days old). All animals were housed in AALAC-accredited Office of Animal Resources facilities at the Harry S. Truman VA Hospital, University of Missouri for a period of 13 weeks. Weaning was chosen as the starting point for the

Weaning (week 4)

Although an effort was made to randomly sort individuals among the cohorts, pre-existing variation in the size and shape of the right hemimandible was observed during week 4. At the time of weaning and before the onset of dietary modification, cohort 1 was observed to have a significantly smaller mandible than cohort 4 (ln mandibular centroid size, p = 0.003) (Fig. 2, Tables S1 and S2 in the online Appendix). The Procrustes distances between cohorts 1 and 2, and cohorts 1 and 4, were also

Discussion

The mammalian mandible can be broadly divided into two functional regions: the ramus, consisting of the articular process and multiple attachment sites for the major masticatory muscles, and the corpus, which supports the teeth (Atchley et al., 1992, Klingenberg et al., 2003a). Within each of these regions, there are multiple distinct modules that have genetic, developmental, and functional underpinnings (Atchley et al., 1985, Atchley et al., 1992, Cheverud et al., 1997, Klingenberg et al.,

Acknowledgments

We thank Scott Maddux for advice on data analysis, and Beth Brainerd, Jason Organ, David Polly and an anonymous reviewer for helpful comments. Chris Vinyard kindly performed the analyses of food material properties. We greatly appreciate the support of the Biomolecular Imaging Center at the Harry S. Truman VA Hospital. Lastly, we thank Olga Panagiotopoulou and José (Pepe) Iriarte-Diaz for the invitation to contribute to this special issue on “Determinants of mammalian feeding system design”.

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    This article is part of a special issue entitled Determinants of Mammalian Feeding System Design.

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