INTRODUCTION

Mammals have evolved remarkable variability in cranio-mandibular design and many morphological and physiological convergent adaptations are mainly related to feeding ecology (Fritz et al. 2009). Browse-plants and grasses exhibit fundamental differences in their properties, such as cell structure, plant chemistry, architecture, and secondary components (e.g., Short 1971; Freeland & Janzen 1974; Rosenthal & Janzen 1979; Demment & van Soest 1985; Cooper & Owen-smith 1986; Shipley 1999), and herbivorous specializations are highly diverse in mammals (Turnbull 1970; Gordon & Illius 1988; Janis & Ehrhardt 1988; Janis & Fortelius 1988; Clauss et al. 2008). Indeed, eutherian and metatherian mammals have evolved a number of parallelisms in their adaptations to dietary type although they show several completely different life history features related to the strategy of reproduction and developmental processes, such as the Metatheria needing for an earlier development of the jaw to suck very early in postnatal life (e.g., Smith 1997; Sánchez-Villagra et al. 2008; Goswami et al. 2012;

Rager et al. 2014, but see, Sánchez-Villagra et al. 2008). Among the similar morphological characters in herbivores, the development of complex occlusal dental surfaces suitable for grinding and crushing and hypsodonty are observed in many grazer taxa among marsupials, rodents, lagomorphs, and ungulates (e.g., Simpson 1953; Fortelius 1985; Janis & Fortelius 1988). Herbivores usually also exhibit relatively large pterygoid and masseteric muscles, contrasting with carnivores that present more developed temporal muscles (Maynard Smith & Savage 1959; Turnbull 1970; Greaves 2008). Among the morphological divergences, a number of differences in relative craniodental proportions between macropodids and ungulates have been observed (see Janis 1990).

On the other hand, comparisons of the occlusion pattern of macropodids and rodents indicate large differences because the occlusion of incisors and molars occurs simultaneously in macropodids but not in rodents (Hiiemae 1971; Weijs & Dantuma 1975; Thorington & Darrow 1996; Lentle et al. 2003).

Among mammals, carnivorans (including placentalsand marsupials) were frequently used as examplesof convergence relating skull morphology andfeeding ecology (e.g., Wroe & Milne 2007; Goswamiet al. 2011; Prevosti et al. 2012). In these taxa,morphological variation was observed principally inthe rostrum and maxilla anatomy, with metatheriancarnivores exhibiting a degree of disparity whichexceeds that of the more speciose eutherian carnivoreradiations (Goswami et al. 2011). However,comparisons considering a more comprehensivesample including herbivore taxa, resulted in an inverseresult (Bennett & Goswami 2013), where theextant marsupial taxa occupied a much smaller areaof morphospace than the placental taxa, supportingthe hypothesis of developmental constraint limitingthe evolution of the marsupial skull (e.g., Wroe & Milne 2007; Goswami et al. 2011; Prevosti et al. 2012). Following these results, we wanted to test whetherthe supposed morphological constraint in marsupialshas an impact on herbivore masticatory adaptations.In this sense, we expect that placentals will showhigher shape variation because their facial region isnot constrained by functional requirements causedby its early development, as occurs in marsupials.

Correlated evolution of traits can impact the morphological evolution of a structure. That correlation could constrain the variation in some features or, conversely, could promote changes in a trait associated to other that is changing (e.g., Olson & Miller 1958; Goswami 2006). Highly correlated, integrated traits may build up a module ("developmental unit” of Atchley & Hall 1991) since they can share genetic sources, and developmental processes and mechanic demands acting on them (Goswami 2006; Klingenberg 2013) that in turn could be more or less integrated to other modules. Modularity refers to differences in the degree of integration of sets of traits within and between them. Mammalian cranium is a complex, highly integrated structure; but given that the integration is not pervasive, the cranium is structured in modules that are relatively independent (Klingenberg 2013). Various models of modularity have been proposed, and among them the most recognized are those that involve two (neurocranium and face), three (face, cranial base and cranial vault) or six modules (cranial base, cranial vault, orbital, anterior oral-nasal, molar and zygomaticpterygoid regions, Lieberman et al. 2000; Goswami 2006; Hallgrímsson et al. 2007; Drake & Klingenberg 2010; Goswami & Finarelli 2016). Alterations of developmental pathways can generate differences in the patterns of modularity and/or integration (e.g., Goswami et al. 2014; Koyabu et al. 2014), so it could be expected that marsupial and placental mammals present different patterns.

In this study case, we took some selected speciesrepresented by macropodid marsupials and caviidrodents, representing appropriate models for thestudy of anatomical correlates in herbivore marsupialsand placentals. Both groups developed severalecological similarities, such as a mostly grazingfeeding habit and the occupation of open andsemi-wooded environments in Australia and SouthAmerica, respectively. They also show a great sizevariation, ranging between 200 g to 90 kg in caviids(Mones & Ojasti 1986; Nowak 1999), and between1 kg to 80 kg in macropodids (Hume et al. 1989). Macropodids are Australia’s dominant mammalianherbivores, similar to caviomorph rodents in theNeotropics (Osborne 2000; Fabre et al. 2013; Cox & Hautier 2015). Macropodids have a long history ofendemism close to 30 Myr in Australia, while caviidsare recorded from 12.5 Myr ago in the Neotropics (Kirsch 1977; Hume et al. 1989; Nowak 1999; Pérez & Pol 2012). In the context of comparison betweenplacental and metatherian herbivores, the analysespresented here represent an important step in orderto understand the impact of feeding ecology and evolutionaryhistory onto morphological evolution. Weexpect not only obvious dierences between clades,mostly attributed to separate phylogenetic stories,but an intra-clade distribution on the morpho-space,attributed to dierent patterns associated to size variationor ecology in each group, as well as variationsin the modularity models of both clades through theobservation of trait correlations.

MATERIAL AND METHODS

Sample

In order to illustrate shape variation of the skull andmandible of the selected species and to study patternsof cranial modularity, we examined 81 adult specimensrepresentative of each family, Caviidae and Macropodidae (Appendix A). In the case of Caviidae, we included the Brazilian guinea pig, Cavia aperea (0.65 kg; Canevari & Vaccaro 2007, N=13), the Patagonian mara, Dolichotis patagonum (8 kg; Campos et al. 2001, N=13), and thecapybara, Hydrochoerus hydrochaeris (50 kg; Mones &Ojasti 1986, N=15). For Macropodidae, we selected theTasmanian pademelon, Thylogale billardieri (9 kg; Watsonet al. 2012, N=13), the swamp wallaby, Wallabia bicolor(15 kg; Nowak 1999, N=11), and the Eastern gray kangaroo, Macropus giganteus (43 kg; Poole 1982, N=16). Although thespecies selection consists of strict herbivores, dierencesin food habits exist among them. For instance, C. apereais a generalist grazer, it feeds on seeds, leaves, stems, andin some cases, roots or tubers (Asher et al. 2004; Kraus et al. 2005); D. patagonum also shows considerable flexibility in adjusting its diet to different ecosystems, but grassesmake up nearly 70% of its diet (Sombra & Mangione 2005);and H. hydrochaeris is principally a grazer, also feedingon aquatic plants (Herrera & Macdonald 1989). Amongherbivore marsupials it also exists a wide range of feedingtypes. Macropus giganteus is a grazer but eat a wide varietyof foliage ranging from grasses to herbs (Strahan 1995); T. billardierii eats mainly both short green grasses andoccasionally taller woody plants, whereas W. bicolor is abrowser (Ellis 2000; Di Stefano & Newell 2008).

Shape analysis

Shape variation was examined through geometric morphometric techniques. Twenty-five and 11 three-dimensional landmark coordinates were used to represent the cranium and the mandible, respectively (Fig. 1; Table 1). Landmark coordinates were collected using a digitizer (Immersion MicroScribe MX; Immersion Corp., San José, CA, USA). We took care in selecting some landmarks with functional homologies among selected species, such as those that represent muscular attachments and the diastema. In such cases, we generated a description of the landmark that is applicable in both families (see Table 1). Raw coordinates of each dataset were put through to a generalized Procrustes analysis in order to remove non-shape variation (differences in location, orientation and scaling; Rohlf 1999; Mitteroecker & Gunz 2009). To summarize and describe the major trends of cranial and mandibular shape variation a principal component analysis (PCA) of the aligned Procrustes coordinates were carried out for cranial and mandible datasets. Because we expected a considerable high amount of variation on the first principal component (PC1), as a consequence of the phylogenetic distance between macropodids and caviids, the information on the following components could be especially important in terms of shape changes not associated to phylogeny. We run and report the results of a Jolliffe cut-off analysis (Jolliffe 2002) in order to test whether shape change along the PCs might be considered significant. Allometric trends in shape variation of cranium and mandible in caviids and macropodids were analyzed through separate (by family) ordinary least squares regression analyses between the aligned Procrustes coordinates and the natural logarithm of the centroid size (i.e., the square root of the summed squared distances from all landmarks to the configuration centroid) of each specimen (Klingenberg 2016). These morphometric analyses were performed using MorphoJ 1.05f (Klingenberg 2013) and Jolliffe cut-off analysis was carried out in Past vers. 2.16 (Hammer et al. 2001).

In addition, we applied the recently proposed method EMMLi (Evaluating Modularity with Maximum Likelihood) to study phenotypic modularity (Goswami & Finarelli 2016). It allows for comparison of hypotheses of di_erent modularity models, and selection of the most probable model, through the assessment of the likelihoods of trait correlation matrices (each modularity model) using the corrected Akaike Information Criterion (Goswami & Finarelli 2016). For each clade, we confronted three commonly recognized models of mammalian cranial modularity: the first one divides the cranium into two modules (face and neurocranium Drake & Klingenberg 2010), the second one divides it into three modules (face, cranial base and vault; see Table 1; e.g., Bookstein et al. 2003; Hallgrímsson et al. 2007; Álvarez et al. 2015) and the third one divides the cranium into six modules (anterior oral-nasal, molar, orbit, zygomatic-pterygoid, vault, and basicranium; see Table 1; Goswami 2006; Goswami & Polly 2010; Goswami & Finarelli 2016). EMMLi gives the values of inter-module and within-module correlations along the selected model; these values allow comparing, between the analyzed clades, which modules are more correlated with each other and the degree of integration of each module. These analyses were carried out using the package EMMLi (Goswami et al. 2016) for R (R Development Team 2016).

RESULTS

In both cranial and mandibular shape analyses, caviids and macropodids were clearly separated in the morphospace defined by the first two principal components. Both groups were separated along the first PC, whereas species within each family were distributed along the second PC mainly according to size variation (Figs. 2, 3).

In the analysis of the cranium, PC1 explained 69.2% of total variation. The main shape changes contributing to the complete separation of caviids and macropodids on this axis involved the configurations of the rostrum, orbit, and zygomatic arch. Caviids, which were located on positive values of PC1 (Fig. 2), present the following features compared with macropodids: the diastema is larger and deeper, the suture between premaxillary and maxillary bones is backward displaced, the orbit has a posterior position, the supraorbital process is more ventrally and posteriorly located, and the postglenoid process is lacking. Also, the zygomatic arch is not laterally expanded (as it is in macropodids), its dorsal margin reaches a lower position with respect to that of macropodids, and its anterior end is at the same level of the anterior end of superior toothrow, whereas in macropodids it is located far, more posteriorly with respect to the anterior end of superior toothrow. Such deep differences are obviously attributed to separate evolutionary history on both groups. PC2 was significant (Jollifee cut-off 0.0036) and explained 13.52% of total shape variation, including flattening of cranium, lengthening of cranial vault, nasals, and tooth rows towards negative values. According to the ordination obtained for both groups, shape changes observed along this axis could be linked with size variation (see below). In the multivariate space of the cranium, caviids showed more dispersion and it occurred mostly following the PC2 direction, whereas macropodids showed more variation on PC1.

In the analysis of the mandible, PC1 explained 78.06% of the total variation. As occurred in the analysis of the cranium, caviids and macropodids were placed in opposite ends of the first axis, showing contrasting features (Fig. 3). Caviids bear a lower coronoid process, higher condyle, and a posteriorly extended angular process compared to macropodids, in which it is shorter and medially reflected. PC2 was also significant (Jollifee cut-off 0.0008) and explained 6.51% of the total variation. Association between shape changes and size, as observed in the cranium, was not as clear for caviids as it was for macropodids. While the latter maintained a similar ordination pattern, in caviids, the largest genus, Hydrochoerus, showed a mandibular shape more similar to that of the smallest, Cavia. Toward negative values, the main changes correspond to the relative shortening of the tooth row, lengthening of diastema, rising of the condyle, and a ventrally wider angular process.

The allometric analysis showed that the cranium of caviids presented the strongest allometric influence, with size explaining more than half of variation, although the mandible showed the weakest pattern of allometric variation. Macropodids also displayed high proportions of shape explained by size, for both the cranium and mandible (Table 2; Figs. 4, 5). Overall, cranial shape changes follow similar tendencies in caviids and macropodids; for increasing size, these changes involved shortening of the cranial vault, advancement of the upper incisor alveolus and the enlargement of the diastema, and lengthening of the paracondylar process. In particular for macropodids, there is a notable dorsal flexion of the rostrum (in its dorsal margin) and a dorsal flattening of the braincase in the larger species. In addition, the zygomatic arch is more dorsally placed, and the maxillary process is more ventrally extended and posteriorly positioned in larger species. In the orbital region, the supraorbital process and the anterior margin of the orbit (i.e., lacrimal bone) are more posteriorly positioned in Macropus, determining a proportionally shorter braincase respect to Wallabia and Thylogale. On the other side, the ventral flexion of the palatine torus (as occurs with the ventral extension of the pterygoid hamulus and the already mentioned maxillary process) is notable in the larger species. Among caviids, larger species show a markedly posteriorly tilted occipital plane and a broad rostrum that is widened in its anterior end. In the orbital region, the supraorbital process is more dorsally located. Mandible shape changes associated with size increase were less obvious in caviids than in macropodids. As a common pattern, changes involved a slightly larger diastema and shortening of the angular process. In macropodids, a higher coronoid process is present in Macropus with respect to Wallabia and Thylogale.

The cranial modularity model selected by the EMMLi analysis was that involving a six-module structure for the cranium (Table 3). Both inter-module and withinmodule correlations resulted in similar values between caviids and macropodids (Table 4) although in caviids the anterior oral-nasal and molar modules are relatively highly integrated while the zygomatic-pterygoid module is the most integrated module among macropodids. Moderate values were recovered for inter-module correlations; the largest values for caviids were obtained for the correlation between molar and zygomatic-pterygoid modules and the oral-nasal and orbit modules, while these last two modules were the most correlated among macropodids (Table 4).

DISCUSSION

The basic bauplan of the mammalian masticatory apparatus is usually characterized as bearing a full dentition specialized to omnivory/carnivory, with a generalized masticatory muscular system in which the temporalis muscle is predominant over the masseteric and pterygoid muscle groups (e.g., Turnbull 1970; O’Lleary et al. 2013). Herbivory, in turn, is linked to specialized morphologies that have been achieved by several mammalian groups in a convergent way. Likewise, rodents (and artiodactyls) represent highly specialized morphologies among mammals that departure far from what is considered to represent the generalized skull morphology among basal placentals (O’Lleary et al. 2013), and macropodids (and the remaining diprotodonts) also represent a specialized morphology respect to basal marsupials (e.g., Russell 1974; Horovitz & Sánchez-Villagra 2003).

In our inter-group comparison (i.e., marsupials and placentals) the divergent morphological configurations between both groups (expected by the phylogenetic legacy) suggest that herbivory can be achieved through different morphological pathways although this specialization could lead to some similarities (see below). Indeed, selection for herbivory may be strong enough to overcome the marsupial constraint on trophic apparatus during early development. Alternatively, even if distant taxa such as marsupials and placentals may present similar developmental processes that rule morphological changes, morphological evolution of their species could show similar directions and thus generate convergence; either due to selection or random drift (see Losos 2011).

However, despite the separate evolutionary history between both groups, and probably responding to overall tendencies in mammals and even vertebrates, there is a similar tendency in cranial shape changes when increasing size (e.g., shortening of the vault, position of the upper incisor alveolus and diastema, and paracondylar process development; e.g., Harvey & Pagel 1988). Caviids and macropodids (as well as artiodactyls) share several traits that are linked to their herbivore habits, such as the presence of a marked diastema that separates the molariform teeth from incisors and their cropping and shearing/grinding functions, respectively (Crompton et al. 2008). At the same time, the superficial part of the masseter muscle is usually enlarged, a condition that has been suggested as facilitating manipulation of food items with the incisors (Woods 1972; Warburton 2009).

Beyond sharing these convergent features, the deep differences between both taxonomic groups, principally summarized in PC1, may not have a single explanation related to the phylogenetic legacy, but also with functional aspects or developmental constraints. Macropodids di_erentiate from caviids by having a shorter diastema related to a greater number of incisive teeth and a di_erent dynamic of tooth replacement (i.e., newcheek teeth erupt, the molars move forward relative to the remainder of the skull; (e.g., Kirkpatrick 1964; Russell 1974; Woods 1982; Lentle et al. 2003), the zygomatic arch expands posteriorly giving space to a well-developed temporalis muscle that attaches to a high coronoid process in the mandible, and an anteriorly positioned orbit that locates it above the anterior root of the zygomatic arch (Figs. 2, 3). Conversely, in rodents, the orbit locates posteriorly in comparison with macropodids, which has been linked to the level of hypsodonty of molariform teeth that requires an increased space for rooting or to the necessity of larger panoramic visual fields to avoid predation (e.g. Solounias et al. 1995; Hautier et al. 2012). In fact, considering that macropodids do not show tooth hypsodonty, di_erences in the orbit position observed in Figs. 2 and 3 would support this hypothesis. The achievement of an enlarged super_cial masseter muscle (which also presents a proper orientation of its fibers for antero-posterior movements, necessary to separate the functions of incisor and molariform teeth) is accomplished in macropodids by the presence of a characteristic maxillary process in the anterior extreme of the zygomatic arch that extends ventrally, whereas in caviids there is a marked posterior extension of the angular process of the mandible and the zygomatic arch is anteriorly displaced (Figs. 2, 3).

The described patterns of shape variation in both clades (i.e., intra-group variation) allowed analyzing morphological diversification related to size variation into each group, considering that both samples show comparable interspecific size variation. Some variation on PC2 of cranial and mandibular morphospaces was size-dependent, and related, among other features, to a tendency to the lengthening of the rostrum. The propensity for small species to be short-faced and large species to be long-faced) seems to be a ‘rule’ which has been reported in vertebrates (see Emerson & Bramble 1993; Wilson & Sánchez-Villagra 2011) and in a large number of mammalian clades including rodents (Hautier et al. 2012; Álvarez et al. 2013, results presented here), antelopes, fruit-bats, mongooses, tree squirrels (Cardini 2013), deer (Merino et al. 2005), monkeys (Singleton 2005; Cardini & Elton 2008), carnivorans (Segura et al. 2013) and large kangaroos (Milne & O’Higgins 2002; Cardini et al. 2015, results presented here). Beyond the strongly different pattern of development in marsupials and placentals (e.g., Goswami et al. 2009), both cladeswould present a common pattern of allometric variation of the rostrum because there is a conserved relative timing of cranial ossification patterns in early mammalian evolution (Sánchez-Villagra et al. 2008) and there are no specific differences in the postnatal allometric growth in marsupials and placentals (Flores et al. 2013, 2015, 2018). Cardini (2013) proposed the need for a well-developed trophic apparatus in large mammals, in order to maintain function and eficiency, beyond their belonging to marsupial or placental clades. However, size increasing (and rostrum increasing) can bring a cascade of metabolic consequences referred to, for instance, the volume of processed food, the size of the dental occlusal surface, etc, which were not deeply discussed. A large component of the facial variation in mammals was associated with their diversity of size. Facial shape can respond to selection by a simple change in body size (e.g., Schluter 1996; Marroig & Cheverud 2005; Álvarez et al. 2013). A large proportion of the facial variation in both herbivore groups may be associated with size diversification (as was proposed for caviomorph rodents in Álvarez et al. 2013).

These comparable allometric (and developmental) patterns observed among rodents and macropodids may have a correlate with the integration patterns depicted by these groups. It has been shown that the large functional differences between placentals and marsupials regarding the oral apparatus during early developmental stages (i.e., di_ering feeding strategies of neonates), clearly influences on the amount of morphological integration among cranium parts in both groups (e.g., Goswami et al. 2009, 2012) and it is also associated to the distinct levels of disparity found between placentals and marsupials (e.g., Bennett & Goswami 2013). Both in caviids and macropodids, the largest value of intermodule correlation was found for the oral-nasal and orbit modules that include anatomical landmarks belonging to the viscerocranium that shows common developmental patterns across marsupials (e.g.; Flores et al. 2013, 2015, 2018). However, the intra-module correlation values obtained in the present report were somewhat variable between both groups. Interestingly, we reported relatively low values of within-module correlation for the oral-nasal and molar modules in macropodids. This gives support to the finding of Goswami et al. (2012) that in the marsupial analyzed by them (Monodelphis) the levels of integration of the oral region decreases along the growth of individuals. In addition, Goswami et al. (2011) showed that carnivorous marsupials exhibited higher morphological disparity of the oral region compared with placentals, which could be supported herein because the shape variation on the PC1 is higher in macropodids, although our sample is still exploratory for a more general conclusion. In contrast, in caviids, the oral-nasal and molar modules are highly integrated. Such result could suggest some constraints related to the presence of the diastema and the development of incisors, or a probable allometric e_ect, as the cranial shape variation in caviids was explained by size in high proportion (>50%; Table 2). However, it is interesting to note that the amount of shape variation of the mandible on PC1 was higher in caviids than in macropodids. In general terms, and in agreement with previous studies (e.g., Prevosti et al. 2012; Bennett & Goswami 2013), much lower morphospace occupation was found among macropodids compared to that observed for caviids. Thus, although the study case reported here focused on an exploratory inter-generic variation within two families, these results also give some support to the statement that marsupials evolved through a constrained morphological repertoire (Sears 2004; Goswami et al. 2011; Prevosti et al. 2012; Bennett & Goswami 2013). However, to be quite sure of this pattern, most members, both extant and extinct, of these families should be included in further studies since there are some macropodid taxa that could potentially increase shape variation (e.g., †Halmaturus, †Protemnodon, †Sthenurus), considering previous reports (Bennett & Goswami 2013). In a broader taxonomic context, remarkable amplitude of the morpho-space of herbivorous marsupials (possibly comparable to placental) could be expected, considering highly modified forms such as Phalangeriformes or Vombatiformes (Wilson & Mittermeier 2015).

In order to reach a better understanding of the evolutionof specializations in the herbivore guilds, it is necessary toconduct comprehensive studies on a wider range of mammalianclades focusing on shape variation analyses andestimation of morphological disparities among herbivoremammals, and its comparison with carnivores. Studies on awider range of species may reveal cases of morphological orfunctional convergences, which may aid the understandingof the evolution and specializations to particular feedingniches.

Acknowledgements

The authors thank to the personnel of the collectionswho allowed the access to the material: D. H. Verziand A. I. Olivares (Museo de La Plata, Argentina), S.Lucero (Museo Argentino de Ciencias Naturales, BuenosAires, Argentina), S. Bogan (Fundación Félix de Azara,Universidad Maimónides, Buenos Aires, Argentina), R.Voss (American Museum of Natural History, New York),B. Stanley and B. Patterson (Field Museum of Natural History, Chicago) and K. Helgen andD. Lunde (Smithsonian Institution,Washington DC).We thank D. Melo for methodologicaladvice. We thank two anonymous reviewersfor their comments that greatly improved the original manuscript. The authors declare no conflicts of interest.This study was supported by an external fellowship of the CONICET to DAF, and represents a contribution to grants PICT-2012-1583 of the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) to DAF, PICT-2013-2672to AA; PICT-2008-1798 and PICT 2015-2389 to N. Giannini,and PIP 0270 (CONICET) to D.H. Verzi.

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