Simpsonian adaptive radiation occurs through the “more or less simultaneous divergence of numerous lines all from much the same ancestral adaptive type into different, also diverging adaptive zones” (13). The results of our study do not support the hypothesis that the diversity in diet of the lemuriform clade emerged as a product of Simpsonian style adaptive radiation at the beginning of the Eocene, either as a response to dispersal to Madagascar or as a signal of cladogenesis. There is no signal of elevated rates of evolution in any of the three dental topography metrics, no early partitioning of morphological disparity, and relatively low rates of adaptive evolution away from the ancestral frugivorous ecology and toward folivory. Evidence for a dietary adaptive radiation of lemurs during the Oligocene is mixed. High rates of transition toward folivory are observed during the first 10 Ma of this interval, which is consistent with increased exploitation of defended plant resources in expanding and diversifying forests. However, evolutionary modelling and MDI fail to indicate rapidly divergent evolution into distinct ecological niches, at least as captured by the evolution of tooth shape descriptors.
Model for lemur dietary evolution
Reconstructions of historical dietary ecology and molar morphology allow the tracing of a more complex model for lemur dietary evolution (Fig. 3, 5). The ancestral lemuriform appears to have resembled ancestral lorisiforms and fossil stem strepsirrhines in its molar morphology, and likely pursued a dietary ecology of mixed frugivory, gummivory, and insectivory. Cheirogaleids have continued to occupy this ecospace (48,49). The clade uniting lemurids and indriids (including the subfossil families Archaeolemuridae and “Palaeopropithecidae”) substantially modified the ancestral strepsirrhine molar morphology in reducing the strength of the protocristid and opening the talonid and trigonid basins. This tooth morphology approaches a more bilophodont morphology, a configuration that combines “blades” for slicing leaves with “wedges” for forcing open seeds (49,50). The evolution of a more bilophodont morphology at this lemurid + indriid node may indicate an important shift toward a mixed diet of fruits enclosed in hard rinds (“defended” fruits), seeds, and leaves.
At this juncture, lemurids and their sister group of indriids + archaeolemurids took divergent paths. The ancestral lemurid broadly resembles Lemur catta in reconstructed tooth shape, which may provide a model for the ecological origins of the group. L. catta consumes a mixed, seasonally shifting diet of leaves and fruits, including many defended fruits enclosed in hard rinds (51). From this generalist ancestor, two lemurid dietary strategies diverged. Eulemur, Varecia, and the extinct Pachylemur evolved toward specializations on fleshy fruits (52–54). Adaptations toward processing soft fruits include the reduction of the trigonid and expansion of the talonid basin, the reduction of the entoconid, and the incorporation of the entoconid into a continuous buccal crest without a talonid notch. Hapalemur and Prolemur, alternatively, evolved toward folivory, and in particular the exploitation of reedy grasses, through the enclosure of the trigonid and talonid basins in high, thickly developed crests (55,56).
The reconstructed LCA of indriids and archaeolemurids is similar in dental morphology to the LCA of lemurids + indriids and this ancestral form may have exploited a diet broadly similar to Propithecus, combining fruits, seeds, and leaves in seasonally shifting combinations (54,57–59). Members of this clade then appear to diverge in their adaptive strategies. The LCA of archaeolemurids shares adaptations for the exploitation of hard foods with the terminal taxa Archaeolemur and Hadropithecus (60,61). The ancestral indriid may have shifted toward the exploitation of leaves, as indicated by the dietary ecology inferred from the reconstructed dental topography metrics at this node, while retaining adaptations for processing seeds and fruit. Molar features characteristic of indriids are present in this reconstructed ancestor, including a reduced protocristid with an expanded, open trigonid basin approaching the talonid in area, a prominent entoconid with a well-developed talonid notch, and bucco-lingually oriented crests connecting the protoconid and metaconid and entoconid and hypoconid. It is possible that these features evolved in an ancestor for which seed predation was a more important dietary activity than folivory. Highly specialized folivores like Indri, Avahi, and some of the subfossil “palaeopropithecids” arise later within this radiation (58,62,63).