Paleoenvironmental inferences on the Late Miocene hominoid-bearing site of Can Llobateres (NE Iberian Peninsula): An ecometric approach based on functional dental traits.

Hispanopithecus laietanus from the Late Miocene (9.8 Ma) of Can Llobateres 1 (CLL1; Vallès-Penedès Basin, NE Iberian Peninsula) represents one of the latest occurrences of fossil apes in Western mainland Europe, where they are last recorded at ∼9.5 Ma. The paleoenvironment of CLL1 is thus relevant for understanding the extinction of European hominoids. To refine paleoenvironmental inferences for CLL1, we apply ecometric models based on functional crown type (FCT) variables-a scoring scheme devised to capture macroscopic functional traits of occlusal shape and wear surfaces of herbivorous large mammal molars. Paleotemperature and paleoprecipitation estimates for CLL1 are provided based on published regional regression models linking average FCT of large herbivorous mammal communities to climatic conditions. A mapping to Whittaker's present-day biome classification is also attempted based on these estimates, as well as a case-based reasoning via canonical variate analysis of FCT variables from five relevant biomes. Estimates of mean annual temperature (25 °C) and mean annual precipitation (881 mm) classify CLL1 as a tropical seasonal forest/savanna, only in partial agreement with the canonical variate analysis results, which classify CLL1 as a tropical rainforest with a higher probability. The former biome agrees better with previous inferences derived from fossil plants and mammals, as well as preliminary isotopic data. The misclassification of CLL1 as a tropical forest is attributed to the mixture of forest-adapted taxa with others adapted to more open environments, given that faunal and plant composition indicates the presence of a dense wetland/riparian forest with more open woodlands nearby. The tested FCT ecometric approaches do not provide unambiguous biome classification for CLL1. Nevertheless, our results are consistent with those from other approaches, thus suggesting that FCT variables are potentially useful to investigate paleoenvironmental changes through time and space-including those that led to the extinction of European Miocene apes.

A revised (earliest Vallesian) age for the hominoid-bearing locality of Can Mata 1 based on new magnetostratigraphic and biostratigraphic data from Abocador de Can Mata (Vallès-Penedès Basin, NE Iberian Peninsula).

The Abocador de Can Mata (ACM) composite stratigraphic sequence (els Hostalets de Pierola, Vallès-Penedès Basin, NE Iberian Peninsula) has yielded a diverse primate assemblage from the late Aragonian (Middle to Late Miocene). Detailed litho-, bio-, and magnetostratigraphic control has enabled an accurate dating of these fossil remains. Comparable data, however, were lacking for the nearby locality of Can Mata 1 (CM1), which yielded a dryopithecine canine of a female individual. Given the lack of hipparionin equids and giraffids, CM1 has been correlated to the latest Aragonian (Mammal Neogene [MN] zone MN7+8). Here we revise the age of CM1 based on fieldwork and associated paleomagnetic samplings undertaken in 2018-2021. Our results extend the ACM composite sequence upward and indicate that CM1 correlates to the earliest Vallesian (MN9). The updated ACM sequence has a thickness of ∼300 m and comprises 12 magnetozones correlated to subchrons C5Ar.1r to C5n.2n (∼12.6-11.1 Ma; latest MN6 to earliest MN9, late Aragonian to earliest Vallesian). CM1 is correlated to C5r.1r (11.146-11.056 Ma), with an interpolated age of 11.11 Ma, thus postdating the dispersal of hipparionin horses into the Vallès-Penedès Basin-which is correlated to the previous subchron C5r.1n, with an interpolated age of 11.18 Ma, and by definition marks the beginning of the Vallesian. CM1 also minimally postdates the earliest record of giraffids at ACM-representing their earliest well-dated occurrence in the basin-being correlated to C5r.1n with an interpolated age of 11.11 Ma. We conclude that CM1 has an earliest Vallesian (MN9) age of ∼11.1 Ma, intermediate between the Aragonian dryopithecins and the Vallesian hispanopithecins. Ongoing paleontological surveillance at ACM thus offers the prospect to yield additional earliest Vallesian ape remains, which are essential to clarify their taxonomic allocation as well as to confirm whether hispanopithecins evolved locally from dryopithecins rather than immigrating from elsewhere during MN9.

Palaeoecological differences underlie rare co-occurrence of Miocene European primates.

BACKGROUND: The two main primate groups recorded throughout the European Miocene, hominoids and pliopithecoids, seldom co-occur. Due to both their rarity and insufficiently understood palaeoecology, it is currently unclear whether the infrequent co-occurrence of these groups is due to sampling bias or reflects different ecological preferences. Here we rely on the densely sampled primate-bearing sequence of Abocador de Can Mata (ACM) in Spain to test whether turnovers in primate assemblages are correlated with palaeoenvironmental changes. We reconstruct dietary evolution through time (ca. 12.6-11.4 Ma), and hence climate and habitat, using tooth-wear patterns and carbon and oxygen isotope compositions of enamel of the ubiquitous musk-deer Micromeryx. RESULTS: Our results reveal that primate species composition is strongly correlated with distinct environmental phases. Large-bodied hominoids (dryopithecines) are recorded in humid, densely-forested environments on the lowermost portion of the ACM sequence. In contrast, pliopithecoids inhabited less humid, patchy ecosystems, being replaced by dryopithecines and the small-bodied Pliobates toward the top of the series in gallery forests embedded in mosaic environments. CONCLUSIONS: These results support the view that pliopithecoid primates preferred less humid habitats than hominoids, and reveal that differences in behavioural ecology were the main factor underpinning their rare co-occurrence during the European Miocene. Our findings further support that ACM hominoids, like Miocene apes as a whole, inhabited more seasonal environments than extant apes. Finally, this study highlights the importance of high-resolution, local investigations to complement larger-scale analyses and illustrates that continuous and densely sampled fossiliferous sequences are essential for deciphering the complex interplay between biotic and abiotic factors that shaped past diversity.

Calibration of life history traits with epiphyseal closure, dental eruption and bone histology in captive and wild red deer.

The study of skeletochronology and bone tissue as a record of information on ontogenetic stages and events is widely used for improving the knowledge about life histories (LHs) of extinct and extant vertebrates. Compared with dinosaurs and extant reptiles, mammalian bone histology has received little attention. Here, we calibrate for the first time bone and dental age with histological bone characteristics and LH stages in ontogenetic series of red deer. We rely on known LHs of different aged individuals of captive Cervus elaphus hippelaphus from Austria to correlate epiphyseal closure, dental eruption pattern, bone growth marks and bone tissue patterns in femora and tibiae, and of wild Cervus elaphus hispanicus from Spain. Our data show that females (of both subspecies) attain skeletal maturity earlier than males. At this moment, epiphyseal closure (in femora and tibiae) and dental eruption are complete and long bones start to deposit an external fundamental system. The results also show that the attainment of reproductive maturity in red deer occurs slightly before skeletal maturity.

Understanding climate's influence on the extinction of Oreopithecus (late Miocene, Tusco-Sardinian paleobioprovince, Italy).

Despite its long history of scientific study, the causes underlying the extinction of the insular hominoid Oreopithecus bambolii are still a matter of ongoing debate. While some authors consider intense tectonism and invading species the cause of its extinction ca. 6.7 Ma, others propose climatic change as the main contributing factor. We rely on long-term patterns of tooth wear and hypsodonty of the Baccinello and Fiume Santo herbivore-faunas to reconstruct changes in habitat prior to, during and after the extinction. While a mosaic of habitats was represented in Baccinello V1 (as shown by a record of browsers, mixed feeders and species engaged in grazing), more closed forests (higher proportion of browsers, shortage of mixed feeders and lack of grazers) characterised Baccinello V2. Finally, there was a partial loss of canopy cover and development of open-patches and low-abrasive grasses in Baccinello V3 (as denoted by new records of taxa involved in grazing)-although still dominated by a forested habitat (since browse was a component in all diets). Our results provide evidence for two perceptible shifts in climate, one between 8.1 and 7.1 Ma and other ca. 6.7 Ma, though this latter was not drastic enough to lead to intensive forest loss, substantially alter the local vegetation or affect Oreopithecus lifestyle-especially if considering the growing evidence of its versatile diet. Although the disappearance of Oreopithecus is complex, our data reject the hypothesis of environmental change as the main factor in the extinction of Oreopithecus and Maremma fauna. When our results are analysed together with other evidence, faunal interaction and predation by invading species from mainland Europe seems to be the most parsimonious explanation for this extinction event. This contrasts with European hominoid extinctions that were associated with major climatic shifts that led to environmental uniformity and restriction of the preferred habitats of Miocene apes.

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.

European pliopithecid diets revised in the light of dental microwear in Pliopithecus canmatensis and Barberapithecus huerzeleri.

Pliopithecinae and Crouzeliinae (Primates: Pliopithecidae) are distinguished dentally by the sharper crests, more compressed cusps, larger foveae, and narrower molars of the latter. Traditionally, such differences were qualitatively related to increased folivory in crouzeliines. This was subsequently disproved by microwear and shearing crest analyses, indicating that all pliopithecids were soft-fruit eaters, except for the more folivorous crouzeliine Barberapithecus. This seems however at odds with the occlusal morphology of the latter, intermediate between those of Pliopithecus and the more derived crouzeliine Anapithecus. To further assess dietary evolution in this group, we report results of dental microwear for two Iberian pliopithecids: Pliopithecus canmatensis, from several Abocador de Can Mata localities (11.8-11.7 Ma, MN8), and Barberapithecus huerzeleri from Castell de Barberà (ca. 11.2-10.5 Ma, MN8, or MN9). Contrary to previously published results, our analyses suggest that all pliopithecids, including Barberapithecus, had a frugivorous diet with a significant sclerocarpic component-apparently more marked in some pliopithecines (such as P. canmatensis) than in the crouzeliine Anapithecus. If our interpretation is correct, it would mean that, within the framework of a frugivorous diet with some hard-object feeding, crouzeliine dental evolution would have been driven by selection pressures towards increased soft-fruit consumption instead of folivory. Dental differences between pliopithecids and hominoids with a significant sclerocarpic component (i.e., orangutans) might be related to phylogenetic constraints, different food-processing methods and/or fracture toughness of hard foods consumed. Although additional research would be required, results suggest that dietary niche partitioning played a significant role in the radiation of European pliopithecids.

Evidence of correlated evolution of hypsodonty and exceptional longevity in endemic insular mammals.

Here, we test whether the increase in tooth height in insular endemics results from the expansion of the dietary niche under resource limitation, as widely considered, or whether it represents an investment in dental durability in response to the selection for extended longevity under low levels of extrinsic mortality. We tested these hypotheses in the extremely hypsodont fossil bovid Myotragus balearicus from the Balearic Islands, an ideal model to study the evolutionary trends on islands. Dental abrasion was significantly lower in the insular bovid than in highly hypsodont continental artiodactyls, suggesting that feeding habits are not the sole driving force behind increased crown height. However, the estimated longevity for M. balearicus based on dental durability was two times that predicted from body mass. Survivorship curves confirm that an extraordinarily large number of individuals approached the longevity of the species. Our results, hence, provide evidence that hypsodonty in insular endemics is the outcome of selection for increased durability of the permanent dentition in association with an extended lifespan. In the context of insularity, our results lend additional support to the disposable soma theory of ageing confirming the dependency of somatic maintenance and repair on lifespan, and its control by resource availability and extrinsic mortality.

Ruminant inner ear shape records 35 million years of neutral evolution.

Extrinsic and intrinsic factors impact diversity. On deep-time scales, the extrinsic impact of climate and geology are crucial, but poorly understood. Here, we use the inner ear morphology of ruminant artiodactyls to test for a deep-time correlation between a low adaptive anatomical structure and both extrinsic and intrinsic variables. We apply geometric morphometric analyses in a phylogenetic frame to X-ray computed tomographic data from 191 ruminant species. Contrasting results across ruminant clades show that neutral evolutionary processes over time may strongly influence the evolution of inner ear morphology. Extant, ecologically diversified clades increase their evolutionary rate with decreasing Cenozoic global temperatures. Evolutionary rate peaks with the colonization of new continents. Simultaneously, ecologically restricted clades show declining or unchanged rates. These results suggest that both climate and paleogeography produced heterogeneous environments, which likely facilitated Cervidae and Bovidae diversification and exemplifies the effect of extrinsic and intrinsic factors on evolution in ruminants.

Taphonomic and spatial analyses from the Early Pleistocene site of Venta Micena 4 (Orce, Guadix-Baza Basin, southern Spain).

Venta Micena is an area containing several palaeontological sites marking the beginning of the Calabrian stage (Early Pleistocene). The richness of the fossil accumulation including species of Asian, African and European origin, makes Venta Micena a key site for the the palaeoecological and palaeoenvironmental study of southern Europe during the Early Pleistocene. Thus, research has been focused on Venta Micena 3, which was originally interpreted as a single palaeosurface associated with a marshy context, in which most of the fauna was accumulated by Pachycrocuta brevirostris. Recent excavations have unearthed a new site, Venta Micena 4, located in the same stratigraphic unit (Unit C) and in close proximity to Venta Micena 3. Here we show the first analyses regarding the taphonomic and spatial nature of this new site, defining two stratigraphic boundaries corresponding to two different depositional events. Furthermore, the taphonomic analyses of fossil remains seem to indicate a different accumulative agent than Pachycrocuta, thus adding more complexity to the palaeobiological interpretation of the Venta Micena area. These results contribute to the discussion of traditional interpretations made from Venta Micena 3.

Ancestral feeding state of ruminants reconsidered: earliest grazing adaptation claims a mixed condition for Cervidae.

BACKGROUND: Specialised leaf-eating is almost universally regarded as the ancestral state of all ruminants, yet little evidence can be cited in support of this assumption, apart from the fact that all early ruminants had low crowned cheek teeth. Instead, recent years have seen the emergence evidence contradicting the conventional view that low tooth crowns always indicate leaf-eating and high tooth crowns grass-eating. RESULTS: Here we report the results of two independent palaeodietary reconstructions for one of the earliest deer, Procervulus ginsburgi from the Early Miocene of Spain, suggesting that despite having lower tooth crowns than any living ruminant, this species included a significant proportion of grass in its diet. CONCLUSION: The phylogenetic distribution of feeding styles strongly supports that leaf-grass mixed feeding was the original feeding style of deer, and that later dietary specialization on leaves or grass occurred independently in several lineages. Evidence for other ruminant clades suggests that facultative mixed feeding may in fact have been the primitive dietary state of the Ruminantia, which would have been morphologically expressed only under specific environmental factors.

MicroWeaR: A new R package for dental microwear analysis.

Mastication of dietary items with different mechanical properties leaves distinctive microscopic marks on the surface of tooth enamel. The inspection of such marks (dental microwear analysis) is informative about the dietary habitus in fossil as well as in modern species. Dental microwear analysis relies on the morphology, abundance, direction, and distribution of these microscopic marks. We present a new freely available software implementation, MicroWeaR, that, compared to traditional dental microwear tools, allows more rapid, observer error free, and inexpensive quantification and classification of all the microscopic marks (also including for the first time different subtypes of scars). Classification parameters and graphical rendering of the output are fully settable by the user. MicroWeaR includes functions to (a) sample the marks, (b) classify features into categories as pits or scratches and then into their respective subcategories (large pits, coarse scratches, etc.), (c) generate an output table with summary information, and (d) obtain a visual surface-map where marks are highlighted. We provide a tutorial to reproduce the steps required to perform microwear analysis and to test tool functionalities. Then, we present two case studies to illustrate how MicroWeaR works. The first regards a Miocene great ape obtained from through environmental scanning electron microscope, and other a Pleistocene cervid acquired by a stereomicroscope.

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.

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 today's 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. © 2016 Wiley Periodicals, Inc.

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

Miocene small-bodied anthropoid primates from Africa and Eurasia are generally considered to precede the divergence between the two groups of extant catarrhines­hominoids (apes and humans) and Old World monkeys­and 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).

Key innovations in ruminant evolution: a paleontological perspective.

Key innovations are newly acquired structures that permit the performance of a new function and open new adaptive zones, and are, therefore, of paramount significance for understanding the history of the Ruminantia, particularly its diversification through the Miocene. Here we review and discuss what is known about these evolutionary novelties, with special emphasis on the appearance and evolution of cranial appendages and high-crowned (or hypsodont) teeth. Cranial appendages probably favored the diversification of pecorans by being structures strongly related to sexual selection, whereas the acquisition of hypsodont teeth could have expanded potential dietary breadth and allowed species to extend diets into the grazing range without eliminating browsing as a potential diet. When analyzed in conjunction with patterns of faunal diversity and in the context of climatic changes, it seems that the overall view that ruminant cranial appendages and hypsodonty may have started responding to increased patterns of seasonality and the opening-up of ecosystems is roughly valid. Instead, they occurred through several distinct pulses and varied widely among continents. This review is, to our knowledge, the first to highlight that the evolution of these innovations has been far from constant and uniform through time. Furthermore, we identify that both a first attempt to increase hypsodonty starting in the early Miocene and a first evolution of antlers and pronghorns were interrupted as a consequence of wide climatic fluctuations in the early-middle Miocene transition.

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.

Systematics and taxonomy of the Spanish Anchitheriinae, and their relationship with regional climate changes: a comment on Eronen et al.

In a recent paper, Eronen et al. (2010; hereafter EEFJ) observe differences in occlusal morphology, tooth crown height, and mesowear pattern between populations of the Miocene tridactyl equid Anchitherium from Spain and Germany, proposing that Spanish Anchitherium underwent adaptive evolution to local or regional arid conditions. However, these authors do not take into account the actual diversity of Iberian representatives of Anchitherium, or the fact that the Spanish fossils cover a wider temporal and geographical range than those from Germany. For these reasons, we suggest that their subsequent statistical work should be reconsidered.