Daniel DeMiguel

Dietary innovations spurred the diversification of ruminants during the Caenozoic

Global climate shifts and ecological flexibility are two major factors that may affect rates of speciation and extinction across clades. Here, we connect past climate to changes in diet and diversification dynamics of ruminant mammals. Using novel versions of Multi-State Speciation and Extinction models, we explore the most likely scenarios for evolutionary transitions among diets in this clade and ask whether ruminant lineages with different feeding styles (browsing, grazing and mixed feeding) underwent differential rates of diversification concomitant with global temperature change. The best model of trait change had transitions from browsers to grazers via mixed feeding, with appreciable rates of transition to and from grazing and mixed feeding. Diversification rates in mixed-feeder and grazer lineages tracked the palaeotemperature curve, exhibiting higher rates during the Miocene thermal maxima. The origination of facultative mixed diet and grazing states may have triggered two adaptive radiations—one during the Oligocene–Miocene transition and the other during Middle-to-Late Miocene. Our estimate of mixed diets for basal lineages of both bovids and cervids is congruent with fossil evidence, while the reconstruction of browser ancestors for some impoverished clades—Giraffidae and Tragulidae—is not. Our results offer model-based neontological support to previous palaeontological findings and fossil-based hypothesis highlighting the importance of dietary innovations—especially mixed feeding—in the success of ruminants during the Neogene.

Miocene small-bodied ape from Eurasia sheds light on hominoid evolution

Meet your gibbon cousin Apes are divided into two groups: larger-bodied apes, or hominoids, such as humans, chimps, and gorillas; and smaller-bodied hylobatids, such as gibbons. These two lineages are thought to have diverged rather cleanly, sharing few similarities after the emergence of crown hominoids. Alba et al. describe a new ape from the Miocene era that contains characteristics from both hominoids and small-bodied apes (see the Perspective by Benefit and McCrossin). Thus, early small-bodied apes may have contributed more to the evolution of the hominoid lineage than previously assumed. Science, this issue p. 10.1126/science.aab2625; see also p. 515 Early small-bodied apes may have contributed more to the evolution of the hominoid lineage than previously thought. [Also see Perspective by Benefit and McCrossin] INTRODUCTION Reconstructing the ancestral morphotype from which extant hominoids (apes and humans) evolved is complicated by the mosaic nature of ape evolution, the confounding effects of independently evolved features (homoplasy), and the virtual lack of hylobatids (gibbons and siamangs) in the Miocene fossil record. For several decades, small-bodied anthropoid primates from Africa and Eurasia have not played an important role in this debate, because they generally lack the shared derived features of extant catarrhines (hominoids and Old World monkeys) and are thus considered to precede their divergence. Even some small-bodied catarrhines from Africa (dendropithecids), considered to be stem hominoids by some authors, are viewed as more primitive than the larger-bodied stem ape Proconsul. This has led to the assumption that hylobatids are a dwarfed lineage that evolved from a larger-bodied and more great ape–like common ancestor with hominids (great apes and humans). RATIONALE Here we describe a new genus of small-bodied (4 to 5 kg) ape from the Miocene (11.6 Ma), discovered in the Abocador de Can Mata stratigraphic series (Vallès-Penedès Basin, northeast Iberian Peninsula), that challenges current views on the last common ancestor of extant hominoids. This genus is based on a partial skeleton that enables a reliable reconstruction of cranial morphology and a detailed assessment of elbow and wrist anatomy. It exhibits a mosaic of primitive (stem catarrhine–like) and derived (extant hominoid–like) features that forces us to reevaluate the role played by small-bodied catarrhines in ape evolution. RESULTS The new genus retains some features that are suggestive of generalized above-branch quadrupedalism, but it possesses more extensive hominoid-like postcranial features (mostly related to enhanced forearm rotation and ulnar deviation capabilities) than those convergently displayed by atelids. Its overall body plan is more compatible with an emphasis on cautious and eclectic climbing, combined with some degree of below-branch forelimb-dominated suspension (although less acrobatic than in extant gibbons). Its relative brain size implies a monkey-like degree of encephalization (similar to that of hylobatids but below that of great apes), and dental microwear indicates a frugivorous diet. From a phylogenetic viewpoint, the new genus combines craniodental and postcranial primitive features (similar to those of dendropithecids) with multiple derived cranial and postcranial features shared with extant hominoids. Some cranial similarities with gibbons would support a closer phylogenetic link between the new genus and hylobatids. However, this possibility is not supported by the total evidence. A cladistic analysis based on more than 300 craniodental and postcranial features reveals that the new genus is a stem hominoid (preceding the divergence between hylobatids and hominids), although more derived than previously known small catarrhines and Proconsul. CONCLUSION As the first known Miocene small-bodied catarrhine to share abundant derived features with extant hominoids, the new genus indicates a greater morphological diversity than previously recognized among this heterogeneous group, and it provides key insight into the last common ancestor of hylobatids and hominids. Our cladistic results, coupled with the chronology and location of the new genus, suggest that it represents a late-surviving offshoot of a small African stem hominoid that is more closely related to crown hominoids than Proconsul is. These results suggest that, at least in size and cranial morphology, the last common ancestor of extant hominoids might have been more gibbon-like (less great ape–like) than generally assumed. Cranial reconstruction and life appearance. Artist’s representation of the cranial reconstruction (in frontal view) and of the life appearance (in lateral oblique view) of the new genus of small-bodied ape from the Iberian Miocene. [Artwork by M. Palmero] Miocene small-bodied anthropoid primates from Africa and Eurasia are generally considered to precede the divergence between the two groups of extant catarrhines—hominoids (apes and humans) and Old World monkeys—and are thus viewed as more primitive than the stem ape Proconsul. Here we describe Pliobates cataloniae gen. et sp. nov., a small-bodied (4 to 5 kilograms) primate from the Iberian Miocene (11.6 million years ago) that displays a mosaic of primitive characteristics coupled with multiple cranial and postcranial shared derived features of extant hominoids. Our cladistic analyses show that Pliobates is a stem hominoid that is more derived than previously described small catarrhines and Proconsul. This forces us to reevaluate the role played by small-bodied catarrhines in ape evolution and provides key insight into the last common ancestor of hylobatids (gibbons) and hominids (great apes and humans).

Dietary Specialization during the Evolution of Western Eurasian Hominoids and the Extinction of European Great Apes

Given the central adaptive role of diet, paleodietary inference is essential for understanding the relationship between evolutionary and paleoenvironmental change. Here we rely on dental microwear analysis to investigate the role of dietary specialization in the diversification and extinction of Miocene hominoids from Western Eurasian between 14 and 7 Ma. New microwear results for five extinct taxa are analyzed together with previous data for other Western Eurasian genera. Except Pierolapithecus (that resembles hard-object feeders) and Oreopithecus (a soft-frugivore probably foraging opportunistically on other foods), most of the extinct taxa lack clear extant dietary analogues. They display some degee of sclerocarpy, which is most clearly expressed in Griphopithecus and Ouranopithecus (adapted to more open and arid environments), whereas Anoiapithecus, Dryopithecus and, especially, Hispanopithecus species apparently relied more strongly on soft-frugivory. Thus, contrasting with the prevailing sclerocarpic condition at the beginning of the Eurasian hominoid radiation, soft- and mixed-frugivory coexisted with hard-object feeding in the Late Miocene. Therefore, despite a climatic trend towards cooling and increased seasonality, a progressive dietary diversification would have occurred (probably due to competitive exclusion and increased environmental heterogeneity), although strict folivory did not evolve. Overall, our analyses support the view that the same dietary specializations that enabled Western Eurasian hominoids to face progressive climatic deterioration were the main factor ultimately leading to their extinction when more drastic paleoenvironmental changes took place.

Diversification of mammals from the Miocene of Spain

Abstract The mammalian fossil record of Spain is long and taxonomically well resolved, offering the most complete record of faunal change for the Neogene of Europe. We evaluated changes in diversification, composition, trophic structure, and size structure of large mammals over the middle and late Miocene with methods applied to this record for the first time, including ordination of fossil localities to improve temporal resolution and estimation of confidence intervals on taxa temporal ranges. By contrast, analysis within the traditional Mammal Neogene (MN) biochronology obscures important aspects of diversification. We used inferred temporal ranges of species and evaluated per capita rates of origination, extinction, diversification, and turnover over 0.5-Myr time intervals. Three periods of significant faunal change occurred between 12.0 and 5.5 Ma: (1) From 12.0 to 10.5 Ma, elevated origination rates led to an increase in diversity without significant change in ecological structure. Immigrants and geographic-range shifts of species to lower latitudes during an interval of global cooling contributed to these faunal changes. (2) From 9.5 to 7.5 Ma, high extinction rates followed by high origination rates coincided with significant changes in taxonomic composition and ecological structure. These changes represent the Vallesian Crisis, with replacement of a fauna of forest affinities (with frugivores and browsers) by a fauna of open woodlands (with grazers and mixed feeders). (3) From 6.5 to 5.5 Ma, high extinction rates reduced diversity without substantial changes in ecological structure, and large mammal faunas became highly endemic across the northern Mediterranean region. This interval includes the Messinian Salinity Crisis, the desiccation of the Mediterranean basin. Extinction may have been caused by geographic isolation and aridification, with evolution of endemic lineages giving rise to new species in the early Pliocene. These distinct macroevolutionary patterns of faunal change correspond to different geographic scales of inferred climatic and tectonic drivers.

Dietary behaviour and competition for vegetal resources in two Early Miocene pecoran ruminants from Central Spain

ABSTRACT Dietary behaviour and competition for resources are investigated for the small-sized ruminants Andegameryx Ginsburg, 1971 and Procervulus Gaudry, 1877 representatives of two largely distinct states of diversification of pecorans. Results obtained from dental microwear and mesowear methodologies are concordant with a mixed feeder strategy for the taxa from the Early Miocene environments of the Iberian Chain (Central Spain). Further, the Spanish taxa investigated had less abrasive diets than their relatives from others similarly aged localities in Europe. This fact raises an important evolutionary uncertainty concerning the traditional characterization of first pecorans as specialized browsers. Instead, data strongly corroborate the recently proposed notion that some Pecora ruminant lineages were able to consume a mixture of browse and grass, and that were originally facultative mixed feeders. However, there is a large degree of variation of their dental wear features. Species were not dependent on a limited type of vegetation and, consequently, were able to exploit different food resources. Dental wear data seem to indicate that these ruminants did not compete for vegetation. In addition, last Andegameryx and earliest Procervulus apparently had a sufficiently different body size to partition the available vegetation in terms of height above ground level to elude competition. Body size difference coupled with an important degree of dietary opportunism may have been factors necessary for their coexistence.

The First Known Asian Hispanomeryx (Mammalia, Ruminantia, Moschidae)

The first known Asian Hispanomeryx (Mammalia, Ruminantia, Moschidae) Israel M. Sanchez a , Daniel Demiguel b , Victoria Quiralte a & Jorge Morales a a Departamento de Paleobiologia, Museo Nacional de Ciencias Naturales-CSIC, C/ Jose Gutierrez Abascal 2, 28006, Madrid, Spain b Institut Catala de Paleontologia, Universitat Autonoma de Barcelona, Edifici ICP, Campus de la UAB s/n, 08193, Cerdanyola del Valles, Barcelona, Spain

The petrosal bone and bony labyrinth of early to middle Miocene European deer (Mammalia, Cervidae) reveal their phylogeny

Deer (Cervidae) have a long evolutionary history dating back to the Early Miocene, around 19 million years ago. The best known fossils to document this history belong to European taxa, which all bear cranial appendages more or less similar to todays deer antlers. Despite the good fossil record, relationships of the earliest stem deer and earliest crown deer are much debated. This hampers precise calibration against the independent evidence of the fossil record in molecular clock analyses. While much has been written on the Early and Middle Miocene deer, only two phylogenetic analyses have been performed on these taxa to date mostly based on cranial appendage characters. Because the petrosal bone and bony labyrinth have been shown to be relevant for phylogeny in ruminants, we describe for the first time these elements for four iconic early cervids from Europe (Procervulus dichotomus, Heteroprox larteti, Dicrocerus elegans and Euprox furcatus) and include them in a phylogenetic analysis based on the ear region exclusively. The analysis recovered E. furcatus in a sister position to the living red deer (Cervus elaphus). Further, it placed D. elegans in a sister position to Euprox + Cervus and a clade Procervulinae that includes P. dichotomus and H. larteti, in sister position to all other deer. The inclusion of E. furcatus in crown Cervidae, which was previously suggested based on antler morphology, cannot be ruled out here but needs a more comprehensive comparison to other crown deer to be confirmed. J. Morphol. 277:1329–1338, 2016.

Ecological correlates of ghost lineages in ruminants

Abstract Integration between phylogenetic systematics and paleontological data has proved to be an effective method for identifying periods that lack fossil evidence in the evolutionary history of clades. In this study we aim to analyze whether there is any correlation between various ecomorphological variables and the duration of these underrepresented portions of lineages, which we call ghost lineages for simplicity, in ruminants. Analyses within phylogenetic (Generalized Estimating Equations) and non-phylogenetic (ANOVAs and Pearson correlations) frameworks were performed on the whole phylogeny of this suborder of Cetartiodactyla (Mammalia). This is the first time ghost lineages are focused in this way. To test the robustness of our data, we compared the magnitude of ghost lineages among different continents and among phylogenies pruned at different ages (4, 8, 12, 16, and 20 Ma). Differences in mean ghost lineage were not significantly related to either geographic or temporal factors. Our results indicate that the proportion of the known fossil record in ruminants appears to be influenced by the preservation potential of the bone remains in different environments. Furthermore, large geographical ranges of species increase the likelihood of preservation.

Bony labyrinth morphology clarifies the origin and evolution of deer

Deer are an iconic group of large mammals that originated in the Early Miocene of Eurasia (ca. 19 Ma). While there is some consensus on key relationships among their members, on the basis of molecular- or morphology-based analyses, or combined approaches, many questions remain, and the bony labyrinth has shown considerable potential for the phylogenetics of this and other groups. Here we examine its shape in 29 species of living and fossil deer using 3D geometric morphometrics and cladistics. We clarify several issues of the origin and evolution of cervids. Our results give new age estimates at different nodes of the tree and provide for the first time a clear distinction of stem and crown Cervidae. We unambiguously attribute the fossil Euprox furcatus (13.8 Ma) to crown Cervidae, pushing back the origin of crown deer to (at least) 4 Ma. Furthermore, we show that Capreolinae are more variable in bony labyrinth shape than Cervinae and confirm for the first time the monophyly of the Old World Capreolinae (including the Chinese water deer Hydropotes) based on morphological characters only. Finally, we provide evidence to support the sister group relationship of Megaloceros giganteus with the fallow deer Dama.

Disentangling adaptive evolutionary radiations and the role of diet in promoting diversification on islands

Although the initial formulation of modern concepts of adaptive radiation arose from consideration of the fossil data, rigorous attempts to identify this phenomenon in the fossil record are largely uncommon. Here I focus on direct evidence of the diet (through tooth-wear patterns) and ecologically-relevant traits of one of the most renowned fossil vertebrates-the Miocene ruminant Hoplitomeryx from the island of Gargano-to deepen our understanding of the most likely causal forces under which adaptive radiations emerge on islands. Results show how accelerated accumulation of species and early-bursts of ecological diversification occur after invading an island, and provide insights on the interplay between diet and demographic (population-density), ecological (competition/food requirements) and abiotic (climate-instability) factors, identified as drivers of adaptive diversification. A pronounced event of overpopulation and a phase of aridity determined most of the rate and magnitude of radiation, and pushed species to expand diets from soft-leafy foods to tougher-harder items. Unexpectedly, results show that herbivorous mammals are restricted to browsing habits on small-islands, even if bursts of ecological diversification and dietary divergence occur. This study deepens our understanding of the mechanisms promoting adaptive radiations, and forces us to reevaluate the role of diet in the origins and evolution of islands mammals.