Geometric morphometric analyses facilitate linkages between raw data and biological patterns, and can be used to explore morphological shape. Here, it was hypothesized that tooth shape should vary significantly with broad dietary categories among the primate taxa examined here. My results suggest that my hypothesis is supported. Certainly, there is a level of phylogenetic influence in that lemuriform and lorisiform taxa separate along relative warp axes. Thus, phylogenetic relationships should not be discounted in any morphological interpretation (Yamashita,1998a). It would certainly be preferable to additionally investigate the correlation between taxonomic classification, size, and dietary behavior in a multi-factorial interaction model. Unfortunately, given that some of the generic groups are also the only representative of a dietary category (for example, Hapalemur is the only graminivore in the sample), such analyses are not possible statistically due to the limited sample size. Overall, however, the results of the analyses performed here document particular shape trends that are associated with dietary behavior.
Non-Allometric Shape Trends
Although size appears to be a factor in shape variation, ∼74% of the shape variation in the sample did not correlate with size. We can further summarize shape trends along the first three principal components that appear to distinguish between dietary behavioral patterns, rather than body size, as (Fig. 9):
Frugivorous Taxa: Larger talonid crushing areas, produced by the “perpendicular” position of the protolophid and the buccal position of the cristid obliqua. Talonid shearing structures are positioned buccally. It is important to note that Hapalemur (not a frugivorous prosimian) also exhibits a similar morphology, possibly reflecting several phylogenetic or functional factors (as discussed further below).
Folivorous Taxa: More midline shearing structures with an oblique position of the protolophid and the midline position of the cristid obliqua. Hypoflexid crushing areas are generally larger than in frugivores.
Insectivores: A relatively “perpendicular” position of the protolophid (as in frugivores), paired with a more midline position of the cristid obliqua (as in folivores), result in midline shearing structures, albeit broader talonid crushing areas than in folivores.
Figure 9. Summary of shape patterns in dietary groups, (a) frugivory (Eulemur, FMNH 129378); (b) insectivory (Tarsius, FMNH 76860); (c) folivory (Lepilemur, FMNH 5658). Landmark designations follow Fig. 2.
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Variation between taxonomic and dietary groups appears to be driven by the relative positions of the cristid obliqua, the protolophid, and the relative dimensions of the talonid basin. The relative location of shearing and crushing structures has direct implications for functional morphology. Occlusal wear patterns in primates have been discussed at length in the relevant literature (Kay and Hiiemae,1974; Hiiemae,1984) and suggest that during initial stages of Phase I occlusion, the cristid obliqua of the lower molar opposes the postparacrista on the upper molar (Fig. 10). As Phase I occlusion continues, the protolophid of the lower molar also contacts the preprotocrista of the upper molar, ending with the crushing action accomplished through the non-parallel position of the cristid obliqua with the preprotocrista. The function of the cristid obliqua is further constrained by the presence and size of the paraconule on the upper molar.
Figure 10. Illustration of occlusal relationships between the protolophid, cristid obliqua, preprotocristia, and postparacrista in primates (as figured for adapiform Leptadapis magnus) (adapted from Gingerich,1972): (a) positions of the protolophid, cristid oblique, and postparacrista, (b) positions of the protolophid, cristid oblique, and the preprotocrista.
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In individuals with a relatively buccal location of the CO-PRLPHD, the grinding surface of the anterior talonid basin is increased. In addition, as the talonid area increases, the basin area available for retention of food items also increases. On the other hand, a relatively midline location of the CO-PRLPHD may provide increased available crushing surface in the hypoflexid region (buccal to the cristid obliqua) (Fig. 2). Thus, the variation in the location of central shearing, crushing, and grinding complexes (represented by the relative positions of the landmarks examined here) may correlate with differing food properties.
The results provide evidence of additional morphological differences between extant folivorous, frugivorous, and omnivorous prosimians. Establishing morphological differences between insectivores and folivores has been difficult because the physical properties of leaf-structures and exoskeletal structures may demand similar tooth adaptations (tall cusps, expanded shearing surfaces). In many cases, the discernment of folivorous and insectivorous taxa using molar morphology often necessitates the inclusion of body size data (Kay,1975; Kay and Covert,1984). Interpretation of shape, as represented here by the relative location of occlusal landmarks, is not dependent on a known estimate of body size. Future analyses incorporating smaller-sized primate insectivores will further test the shape associations discussed here. In addition, it is necessary to model these patterns against physical properties of food (such as hardness or chemical properties) to explore correlations with shape variation.
Although not mutually exclusive (Lockwood,2007), these results highlight the simultaneous influence of both function and/or phylogeny in morphology. For example, Propithecus is generally classified as “folivorous” while including a large proportion of fruit items (and seeds) in its diet (Meyers and Wright,1993; Hemingway,1995; Dew and Wright,1998; Overdorff and Strait,1998; Simmen et al.,2003; Powzyk and Mowry,2003). Here, Propithecus did not group exclusively with other folivorous taxa (Avahi and Lepilemur) or frugivorous lemurs in the comparison of the first two Principal Components (Fig. 5). Rather, of the two indriids included in the sample, Propithecus did exhibit a tooth with a relatively more buccal CO-PRLPHD and a less oblique protolophid, as in frugivores. Propithecus may exhibit tooth morphology somewhat similar to Avahi as a result of phylogenetic relationships, but this may also reflect a functional convergence to similar shearing requirements (as measured, for example, by shearing quotients). Upon closer inspection, characteristics of an “indriid-type” tooth can vary in some details that may be related to dietary function (particularly the size of crushing areas).
These results for indriids (i.e., the presence of a phylogenetic shape signal overlaid on tooth morphology) would seem to bolster current understanding of evolutionary diversification in indriids, particularly in light of genetic data that suggests folivorous Avahi represents the sister-group of Propithecus and Indri (tooth data not presented here) (Rumpler et al.,1988; Razafindraibe et al.,1997; Roos et al.,2004). Moreover, it should be noted that the folivorous Lepilemur, a lepilemurid, is also characterized by morphology most similar to that of Avahi. This result potentially strengthens the inferred linkage between dietary adaptation and the landmark patterns reported here. Certainly, these inferences must be further explored using material from the Malagasy lemur fossil record (sub-fossil material, for example) before firmer statements regarding the dietary diversification of indriids may be proposed.
Likewise, the shape of the talonid basin observed in Hapalemur may also be a result of both phylogenetic and functional “co-opting” and compromise (Yamashita,1996,1998a,b) in which a feature originally efficient at processing hard seeds and fruit may have also been suitable for efficient mastication of bamboo stems and shoots. Similar functional demands related to “puncture-crushing” for processing both bamboo shoots and fruits/seeds, rather than shearing and grinding (as in folivorous primates) (Seligsohn and Szalay,1978), may be influencing the molar shape patterns reported here. Thus, these data are not incompatible with a phylogenetic hypothesis in which the ancestral lemurid was frugivorous (or graminivorous). Both Hapalemur and Propithecus serve as illustrative cases that suggest phylogeny and function play important, integrated roles in understanding the morphological adaptation, which should not necessarily be considered independently when inferring diet.
Lorisiforms (lorises and galagos), which tend to exhibit a more variable or omnivorous dietary pattern (in particular Perodicticus, Otolemur, and Nycticebus) (Charles-Dominique,1977; Fleagle,1999; Wiens,2002), lie in an intermediate position at the intersection between the ranges of primarily frugivorous, folivorous, and insectivorous taxa. With the exception of Loris, the lorisiform taxa included here overlap in shape trends with one another, which may reflect common phylogenetic patterns or a relative lack of morphological specialization. Although Loris is characterized here as “omnivorous,” it is notable that field observations have documented a high degree of insectivory (Nekaris and Rasmussen,2003). In this analysis, of the omnivorous lorisids, Loris groups most closely with other insectivorous taxa (particularly Tupaia). Otolemur and Nycticebus lie in positions along PC1 and PC2 intermediate between insectivorous taxa and folivorous Lepilemur and indriids (Fig. 5).
Thus, shape patterns in relative cusp and crest positions that overlap taxonomic groups serve to strengthen confidence in the proposed functional correlations suggested here. For example, the overall similarity in insectivore tooth shape (both primate and non-primate) suggests insectivory may be associated with a particular cusp and crest pattern. In addition, functional relationships can also be used to evaluate fossil taxa when utilized in an appropriate phylogenetic context. Morphological data should not be conceived of as static, but rather as a component of ecological data that provides a dynamic picture of adaptation and ecological change. Accordingly, examination of fossil material can result in the development of innovative views of change in community ecology and ecogeography through time (Albrecht et al.,1990; DiMichele,1994; Fleagle and Reed,1996; Lehman et al.,2005). For example, food resource quality, food availability, ecological variability (e.g., wet vs. dry forests), and diminishing soil quality are all continual pressures facing modern lemurs, particularly those dependent on fruits (Ganzhorn et al.,1999). Recent studies have suggested that certain folivorous Lemur species may be more capable of adapting to the change in forest ecology on Madagascar than other more “specialized” taxa (Lehman et al.,2006a,b).
Implications and Summary
The present analysis adds to extensive previous groundwork by investigating patterns of molar shape through exploration of cusp and shearing crest morphology, both components of molar morphology shown to develop early in embryonic development. The benefit of having several methods to pursue is obvious: with different strategies, we are provided the opportunity to test dietary hypotheses from several angles. Several different methods have been previously introduced to address the association between body size and dietary adaptation. For example, measurements of shearing, grinding, and crushing, combined with a measure of body size, appear to be indicative of dietary patterns. Although insectivores and folivores each exhibit parallel patterns of well-developed shearing capacities, only with a measure of body size they are distinguishable (Kay,1975). In general, insectivores also exhibit larger molars in relation to either frugivorous or folivorous primates of similar size. Crown area alone, however, may not sufficiently explain functional differences between primate taxa (Gingerich and Smith,1984).
As the goal of this work was to provide a comparative sample from which to infer dietary behavior in fossil primates, a method that did not require body size was preferable. By employing techniques analyzing the relative location of landmarks as described in the present study, insectivores, folivores, and frugivores were shown to exhibit distinctive shapes without the necessity of body size comparison. Thus, documenting how the relative location of occlusal features of the tooth is effected by size augments the results of Kay (1975) and others, adding a new dimension to the previous investigation of size and molar shape in primates ideally suited to interpreting diet from incomplete fossil remains.
Certainly, it would be short-sighted to suggest that the method presented here for inferring dietary specialization provides a complete picture. Since dietary specialization can be defined at the evolutionary, functional, and behavioral level (Ferry-Graham et al.,2002), various approaches will yield different but complimentary results. For example, information concerning an individual's dietary behavior gained through microwear analysis provides a valuable amount of information regarding the environment and food items available to that individual during a discreet slice of time. However, that individual may exhibit a “specialist” or “generalist” microwear pattern due to ecological constraints, competitive populations, or food availability at a specific point in time, and may not fully reflect its evolutionary background and the adaptive pattern of an ancestral population (Ferry-Graham et al.,2002). Thus, data concerning an individual's lifetime paired with data that reflect upon evolutionary ancestry and adaptation provide a broad picture of ecological change, population behavioral patterns, and morphological adaptation that has been canalized through genetic processes (Polly,2006). Furthermore, although a match in interpretation from all sides may be convenient, we must not overlook the value that these methods provide when they offer counter-interpretations, prodding us to search our functional questions more deeply.
To summarize, it was hypothesized and supported here that primate and non-primate taxa would differ in the relative shape and position of dental structures, and that these differences could be discussed in terms of functional demands placed on the organism as an adaptation to a particular dietary regime.
Using a geometric morphometric approach to investigating the relative position of major occlusal structures in the first lower molar of strepsirrhine primates, the shape trends observed are illustrated in Figs. 9 and 11, and can be summarized as:
Frugivorous Taxa: “Perpendicular” position of the protolophid; buccal position of the cristid obliqua; larger talonid crushing areas.
Folivorous Taxa: Oblique position of the protolophid; midline position of the cristid obliqua; smaller talonid crushing areas; expanded hypoflexid.
Insectivores: “Perpendicular” position of the protolophid; midline cristid obliqua; enlarged talonid and hypoflexid regions.
Figure 11. Summary of shape trends observed in the current study. Symbols indicate: ▵, short, wide tooth, midline CO-PRLPHD, perpendicular protolophid, and large crushing areas (Insectivores); *, long, narrow tooth with oblique protolophid and small crushing areas (Folivores); ○, short, wide tooth, buccal CO-PRLPHD, perpendicular protolophid, and large crushing areas (Frugivores/Graminivores); ⊗, intermediate shape. Branch lengths are not intended to indicate evolutionary time or distance.
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Considering the phylogenetic closeness of extant lemur and lorisiforms to fossil adapiforms, these data provide a broad base from which to compare molar shape and draw conclusions regarding dietary trends. This is not to suggest, however, that adapiforms will be expected to replicate this pattern, or that they are directly ancestral to either living lemurs or lorises. What these data do provide is a comparative baseline from which to propose hypotheses of dietary adaptation and allometric molar-shape scaling trends in adapiforms. The body size of adapiforms has been suggested to be fairly broad [100–6900 g (Fleagle,1999)], and future comparisons will bear out whether adapiforms exhibit similar relationships between size and molar shape. This analysis also suggests that certain features of the molar, such as the position of the protolophid and the cristid obliqua, and the breadth of the anterior talonid basin, may be related to functional demands for shearing and/or crushing. Thus, if differentiation in these features is also documented among adapiforms, further functional hypotheses may be posited regarding this diverse fossil group. These results and the approach used here strongly encourage the collaborative use of several lines of morphological data to reveal the most complete picture of dietary adaptation among fossil primates. Moreover, this approach, in combination with other previously successful methods, suggests that understanding behavioral and ecological diversity is always enhanced by the combination and comparison of different methods.