Francesco Carotenuto

THE SHAPE OF CONTENTION: ADAPTATION, HISTORY, AND CONTINGENCY IN UNGULATE MANDIBLES

Mandibles and teeth of ungulates have been extensively studied to discern the functional significance of their design. Grazing ungulates have deeper mandibles, longer coronoid processes, flatter incisor arcades, and more hypsodont molars in comparison to browsers. If the functional significance of both mandible and teeth shapes is well‐established, it remains uncertain to what extent mandible shapes are really adapted to grazing, meaning that they evolved either to serve their current biological function or just as a structural requirement to accommodate higher crowned molars. Here, we address this question by studying the contribution of phylogeny, hypsodonty, and body size to mandibular shape variation. The mandible shape appeared to be significantly influenced by hypsodonty but not by body size. Interestingly, hypsodonty‐related changes influenced the tooth row in artiodactyls and perissodactyls significantly but in the opposite directions, which is ultimately related to their different digestive strategies. Yet, we obtained a strong phylogenetic effect in perissodactyls, suggesting that their mandible shape should be strongly inherited. The strength of this effect was not significant within artiodactyls (where hypsodonty explained much more variance in mandible shape). Digestive strategy is deemed to interplay with hypsodonty to produce different paths of adaptation to particular diets in ungulates.

Ecological specialization in fossil mammals explains Cope's rule.

Cope’s rule is the trend toward increasing body size in a lineage over geological time. The rule has been explained either as passive diffusion away from a small initial body size or as an active trend upheld by the ecological and evolutionary advantages that large body size confers. An explicit and phylogenetically informed analysis of body size evolution in Cenozoic mammals shows that body size increases significantly in most inclusive clades. This increase occurs through temporal substitution of incumbent species by larger-sized close relatives within the clades. These late-appearing species have smaller spatial and temporal ranges and are rarer than the incumbents they replace, traits that are typical of ecological specialists. Cope’s rule, accordingly, appears to derive mainly from increasing ecological specialization and clade-level niche expansion rather than from active selection for larger size. However, overlain on a net trend toward average size increase, significant pulses in origination of large-sized species are concentrated in periods of global cooling. These pulses plausibly record direct selection for larger body size according to Bergmann’s rule, which thus appears to be independent of but concomitant with Cope’s.

Occupancy, range size, and phylogeny in Eurasian Pliocene to Recent large mammals

Abstract Temporal patterns in species occupancy and geographic range size are a major topic in evolutionary ecology research. Here we investigate these patterns in Pliocene to Recent large mammal species and genera in Western Eurasia. By using an extensively sampled fossil record including some 700 fossil localities, we found occupancy and range size trajectories over time to be predominantly peaked among both species and genera, meaning that occupancy and range size reached their maxima midway along taxon existence. These metrics are strongly correlated with each other and to body size, after phylogeny is accounted for by using two different phylogenetic topologies for both species and genera. Phylogenetic signal is strong in body size, and weaker but significant in both occupancy and range size mean values among genera, indicating that these variables are heritable. The intensity of phylogenetic signal is much weaker and often not significant at the species level. This suggests that within genera, occupancy and range size are somewhat variable. However, sister taxa inherit geographic position (the center of their geographic distribution). Taken together, the latter two results indicate that sister species occupy similar positions on the earths surface, and that the expansion of the geographic range during the existence of a given genus is driven by range expansion of one or more of the species it includes, rather than simply being the summation of these species ranges.

Phylogenetic signal, function and integration in the subunits of the carnivoran mandible

Complex phenotypes could be interpreted as the result of functional integration between identifiable subunits. Common developmental or ecological factors may favour macroevolutionary morphological integration so that functional subunits also covary above the species level. We investigate shape variation and functional integration in two subunits of the mammalian mandible: the corpus and the ramus in a subset of extant terrestrial Carnivora using geometric morphometric and comparative methods. More specifically, we test if corpus and ramus shape exhibit similar degree of homoplasy and if these traits covary above species level. Additionally, broad functional categorisations (predaceous and non predaceous) are investigated to test if differences in morphological variation and integration at macroevolutionary scale occur. Principal components of shape data show a significant phylogenetic signal in both mandibular subunits, with the ramus exhibiting a higher degree of homoplasy than the corpus. Functional groups (predators and non-predators) are significantly distinct in corpus shape, while in the ramus significance emerges only after removing the phylogenetic signal. Partial Least Square shows that mandibular corpus and ramus region covaries above species level even if this trend is not supported when employing comparative methods. Only in a subset of predaceous species covariation still hold. We conclude that mandibular subunits of Carnivora differ considerably in shape among predaceous and non-predaceous species because of the adaptive selection pressure imposed by catching and hold of live prey. This selective process also favoured macroevolutionary integration in predaceous carnivorans.

Rapid action in the Palaeogene, the relationship between phenotypic and taxonomic diversification in Coenozoic mammals

A classic question in evolutionary biology concerns the tempo and mode of lineage evolution. Considered variously in relation to resource utilization, intrinsic constraints or hierarchic level, the question of how evolutionary change occurs in general has continued to draw the attention of the field for over a century and a half. Here we use the largest species-level phylogeny of Coenozoic fossil mammals (1031 species) ever assembled and their body size estimates, to show that body size and taxonomic diversification rates declined from the origin of placentals towards the present, and very probably correlate to each other. These findings suggest that morphological and taxic diversifications of mammals occurred hierarchically, with major shifts in body size coinciding with the birth of large clades, followed by taxonomic diversification within these newly formed clades. As the clades expanded, rates of taxonomic diversification proceeded independently of phenotypic evolution. Such a dynamic is consistent with the idea, central to the Modern Synthesis, that mammals radiated adaptively, with the filling of adaptive zones following the radiation.

Longer in the tooth, shorter in the record? The evolutionary correlates of hypsodonty in Neogene ruminants

The acquisition of hypsodont molars is often regarded as a key innovation in the history of ruminant ungulates. Hypsodont ruminants diversified rapidly during the later Neogene, circa 15–2 Myr ago, and came to dominate the ruminant fossil record in terms of species diversity. Here we show that hypsodont clades had higher speciation and diversification rates than other clades. Hypsodont species had, on average, shorter stratigraphic durations, smaller range size and lower occupancy than non-hypsodont species. Within hypsodont clades, some species were very common and acquired large geographical ranges, whereas others were quite rare and geographically limited. We argue that hypsodont clades diversified in an adaptive radiation-like fashion, with species often splitting cladogenetically while still in the expansive phase of their occupancy history.

Chewing on the trees: Constraints and adaptation in the evolution of the primate mandible.

Chewing on different food types is a demanding biological function. The classic assumption in studying the shape of feeding apparatuses is that animals are what they eat, meaning that adaptation to different food items accounts for most of their interspecific variation. Yet, a growing body of evidence points against this concept. We use the primate mandible as a model structure to investigate the complex interplay among shape, size, diet, and phylogeny. We find a weak but significant impact of diet on mandible shape variation in primates as a whole but not in anthropoids and catarrhines as tested in isolation. These clades mainly exhibit allometric shape changes, which are unrelated to diet. Diet is an important factor in the diversification of strepsirrhines and platyrrhines and a phylogenetic signal is detected in all primate clades. Peaks in morphological disparity occur during the Oligocene (between 37 and 25 Ma) supporting the notion that an adaptive radiation characterized the evolution of South American monkeys. In all primate clades, the evolution of mandible size is faster than its shape pointing to a strong effect of allometry on ecomorphological diversification in this group.

In and Out the Amazonia: Evolutionary Ecomorphology in Howler and Capuchin Monkeys

The impact of environmental variation on phenotypic diversification is one major issue in evolutionary studies. Environmental variation is thought to be a primary factor in evolution, especially at high latitudes. In contrast, tropical areas are traditionally viewed as the cradle where the long-term effects of biological interactions on phenotypic change reside. We analyse patterns of skull shape variation in two New World monkey groups: capuchins and howlers. These two monophyletic clades are exceptionally similar in terms of the geographic distribution of their species. Yet, their body size and diet are different: howler monkeys are large and almost exclusively folivorous, whereas capuchins are small omnivorous. We found that the size, and direction of vectors of phenotypic changes across South American biomes in those clades are not statistically different. This similarity persists after removing the strong impact of allometry in our data. Additionally, partial least squares and comparative analyses confirm that “allometry free” skull shape is influenced to the same set of environmental variables in both clades. This study remarks the paramount importance of both body size and environmental variation on phenotypic evolution.

Progress to extinction: increased specialisation causes the demise of animal clades.

Animal clades tend to follow a predictable path of waxing and waning during their existence, regardless of their total species richness or geographic coverage. Clades begin small and undifferentiated, then expand to a peak in diversity and range, only to shift into a rarely broken decline towards extinction. While this trajectory is now well documented and broadly recognised, the reasons underlying it remain obscure. In particular, it is unknown why clade extinction is universal and occurs with such surprising regularity. Current explanations for paleontological extinctions call on the growing costs of biological interactions, geological accidents, evolutionary traps, and mass extinctions. While these are effective causes of extinction, they mainly apply to species, not clades. Although mass extinctions is the undeniable cause for the demise of a sizeable number of major taxa, we show here that clades escaping them go extinct because of the widespread tendency of evolution to produce increasingly specialised, sympatric, and geographically restricted species over time.

Species accumulation over space and time in European Plio-Holocene mammals

The rate of increase in species number with sampled area is one issue of major interest in ecology. Species number increases with sampled time as well, though this kind of analysis is much rarer in literature. Species-area and species-time relationships have been recently integrated in a single model, which allows studying how time and area interact with each other in determining the cumulative increase in species richness. Here we studied species-area, species-time, and species-time-area relationships in Plio-Holocene large mammals of Western Eurasia, by using an extensive database including 184 species distributed in 685 fossil sites. We found that the increase of species number with time is much higher than with area. When sampling inequality of fossil localities in time and space is accounted for, time and area interact with each other in a negative, though non-linear fashion. The intense climatic changes that characterized the Plio-Holocene period apparently affected both species-area and species-time relationships in large mammals, by increasing the slope of the former during the Pliocene and middle Pleistocene, and of the latter during younger, climatically harsher, late Pleistocene times. This study emphasizes the importance of accounting for time and space in tracing paleodiversity curves.