Response to comment on "Sexual selection promotes giraffoid head-neck evolution and ecological adaptation".

Hou et al. challenged the giraffoid affinity of Discokeryx and its ecology and behavior. In our response we reiterate that Discokeryx is a giraffoid that, along with Giraffa, shows extreme evolution of head-neck morphologies that were presumably shaped by selective pressure from sexual competition and marginal environments.

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.

Sexual selection promotes giraffoid head-neck evolution and ecological adaptation.

The long neck of the giraffe has been held as a classic example of adaptive evolution since Darwin's time. Here we report on an unusual fossil giraffoid, Discokeryx xiezhi, from the early Miocene, which has an unusual disk-shaped headgear and the most complicated head-neck joints in known mammals. The distinctive morphology and our finite element analyses indicate an adaptation for fierce head-butting behavior. Tooth enamel isotope data suggest that D. xiezhi occupied a niche different from that of other herbivores, comparable to the characteristic high-level browsing niche of modern giraffes. The study shows that giraffoids exhibit a higher headgear diversity than other ruminants and that living in specific ecological niches may have fostered various intraspecific combat behaviors that resulted in extreme head-neck morphologies in different giraffoid lineages.

Reassessment of the enigmatic ruminant Miocene genus Amphimoschus Bourgeois, 1873 (Mammalia, Artiodactyla, Pecora).

Amphimoschus is an extinct Eurasian ruminant genus, mostly recorded in Europe, without a close living relative and, hence, an unknown systematic position. This genus is known from around 50 localities from the late early to the middle Miocene. Two species were described during 180 years, but since their first description during the late 19th century and early 20th century, hardly any detailed taxonomic work has been done on the genus. Over the years, extensive collecting and excavating activities have enriched collections with more and more complete material of this still rare and enigmatic animal. Most interestingly, a number of skull remains have been unearthed and are promising in terms of providing phylogenetic information. In the present paper, we describe cranial material, the bony labyrinth, the dentition through 780 teeth and five skulls from different ontogenetic stages. We cannot find a clear morphometric distinction between the supposedly smaller and older species Amphimoschus artenensis and the supposedly younger and larger species A. ponteleviensis. Accordingly, we have no reason to retain the two species and propose, following the principle of priority (ICZN chapter 6 article 23), that only A. ponteleviensis Bourgeois, 1873 is valid. Our studies on the ontogenetic variation of Amphimoschus does reveal that the sagittal crest may increase in size and a supraorbital ridge may appear with age. Despite the abundant material, the family affiliation is still uncertain.

Antiquity and fundamental processes of the antler cycle in Cervidae (Mammalia).

The origins of the regenerative nature of antlers, being branched and deciduous apophyseal appendages of frontal bones of cervid artiodactyls, have long been associated with permanent evolutionary precursors. In this study, we provide novel insight into growth modes of evolutionary early antlers. We analysed a total of 34 early antlers affiliated to ten species, including the oldest known, dating from the early and middle Miocene (approx. 18 to 12 million years old) of Europe. Our findings provide empirical data from the fossil record to demonstrate that growth patterns and a regular cycle of necrosis, abscission and regeneration are consistent with data from modern antlers. The diverse histological analyses indicate that primary processes and mechanisms of the modern antler cycle were not gradually acquired during evolution, but were fundamental from the earliest record of antler evolution and, hence, explanations why deer shed antlers have to be rooted in basic histogenetic mechanisms. The previous interpretation that proximal circular protuberances, burrs, are the categorical traits for ephemerality is refuted.

Insights into the lower torso in late Miocene hominoid Oreopithecus bambolii.

Oreopithecus bambolii (8.3-6.7 million years old) is the latest known hominoid from Europe, dating to approximately the divergence time of the Pan-hominin lineages. Despite being the most complete nonhominin hominoid in the fossil record, the O. bambolii skeleton IGF 11778 has been, for decades, at the center of intense debate regarding the species' locomotor behavior, phylogenetic position, insular paleoenvironment, and utility as a model for early hominin anatomy. Here we investigate features of the IGF 11778 pelvis and lumbar region based on torso preparations and supplemented by other O. bambolii material. We correct several crucial interpretations relating to the IGF 11778 anterior inferior iliac spine and lumbar vertebrae structure and identifications. We find that features of the early hominin Ardipithecus ramidus torso that are argued to have permitted both lordosis and pelvic stabilization during upright walking are not present in O. bambolii However, O. bambolii also lacks the complete reorganization for torso stiffness seen in extant great apes (i.e., living members of the Hominidae), and is more similar to large hylobatids in certain aspects of torso form. We discuss the major implications of the O. bambolii lower torso anatomy and how O. bambolii informs scenarios of hominoid evolution.

Convergent evolution in toothed whale cochleae.

BACKGROUND: Odontocetes (toothed whales) are the most species-rich marine mammal lineage. The catalyst for their evolutionary success is echolocation - a form of biological sonar that uses high-frequency sound, produced in the forehead and ultimately detected by the cochlea. The ubiquity of echolocation in odontocetes across a wide range of physical and acoustic environments suggests that convergent evolution of cochlear shape is likely to have occurred. To test this, we used SURFACE; a method that fits Ornstein-Uhlenbeck (OU) models with stepwise AIC (Akaike Information Criterion) to identify convergent regimes on the odontocete phylogeny, and then tested whether convergence in these regimes was significantly greater than expected by chance. RESULTS: We identified three convergent regimes: (1) True's (Mesoplodon mirus) and Cuvier's (Ziphius cavirostris) beaked whales; (2) sperm whales (Physeter macrocephalus) and all other beaked whales sampled; and (3) pygmy (Kogia breviceps) and dwarf (Kogia sima) sperm whales and Dall's porpoise (Phocoenoides dalli). Interestingly the 'river dolphins', a group notorious for their convergent morphologies and riverine ecologies, do not have convergent cochlear shapes. The first two regimes were significantly convergent, with habitat type and dive type significantly correlated with membership of the sperm whale + beaked whale regime. CONCLUSIONS: The extreme acoustic environment of the deep ocean likely constrains cochlear shape, causing the cochlear morphology of sperm and beaked whales to converge. This study adds support for cochlear morphology being used to predict the ecology of extinct cetaceans.

The bony labyrinth of toothed whales reflects both phylogeny and habitat preferences.

The inner ear of toothed whales (odontocetes) is known to have evolved particular shapes related to their abilities to echolocate and move under water. While the origin of these capacities is now more and more examined, thanks to new imaging techniques, little is still known about how informative inner ear shape could be to tackle phylogenetic issues or questions pertaining to the habitat preferences of extinct species. Here we show that the shape of the bony labyrinth of toothed whales provides key information both about phylogeny and habitat preferences (freshwater versus coastal and fully marine habitats). Our investigation of more than 20 species of extinct and modern odontocetes shows that the semi-circular canals are not very informative, in contrast to baleen whales, while the cochlea alone bears a strong signal. Inner ear shape thus provides a novel source of information to distinguish between morphologically convergent lineages (e.g. river dolphins).

New data on Amynodontidae (Mammalia, Perissodactyla) from Eastern Europe: Phylogenetic and palaeobiogeographic implications around the Eocene-Oligocene transition.

Amynodontidae is a family of Rhinocerotoidea (Mammalia, Perissodactyla) known from the late Early Eocene to the latest Oligocene, in North America and Eurasia. European Amynodontidae are very rare, and all remains belong almost exclusively to a single post-Grande Coupure genus from the Oligocene, Cadurcotherium. The "Grande Coupure" defines an extinctions and dispersal-generated originations event in Europe that is nearly contemporaneous with the Eocene-Oligocene transition. Perissodactyls are one of the major groups affected by this event: Palaeotheriidae went almost extinct during this crisis, whereas Rhinocerotidae appeared for the first time in Europe. Study of fossiliferous Eastern-European localities from this age is crucial for the understanding of this crisis. We report here three new localities of Amynodontidae in Eastern Europe. Two of them are dated from the Eocene (Morlaca, Romania; Dorog, Hungary), whereas the other is either Late Eocene or Early Oligocene (Dobârca, Romania). The skull from this latter locality belongs unexpectedly to the same individual as a previously described mandible attributed to "Cadurcodon" zimborensis. As a result, this specimen can be allocated to its proper locality, Dobârca, and is assigned to a new genus, Sellamynodon gen. nov. It is characterised by an extraordinary growth of the nuchal crest, a unique character among amynodontids. Along with this remarkable material from Dobârca, two specimens from another Romanian locality, Morlaca, have been recently discovered and are dated from the Late Eocene. They belong, as well as new material from Dorog (Middle Eocene, Hungary), to the genus Amynodontopsis, also found in North America. The new Hungarian material represents the earliest occurrence of Amynodontidae in Europe. New phylogenetic hypotheses of Rhinocerotoidea are proposed, including the new material presented here, and show that Amynodontidae may be closer to the polyphyletic family 'Hyracodontidae' than to Rhinocerotidae. Amynodontidae, with their deep preorbital fossa and extremely reduced premolars, display in fact a very derived condition, compared to rhinocerotids.

Micromeryx? eiselei-A new moschid species from Steinheim am Albuch, Germany, and the first comprehensive description of moschid cranial material from the Miocene of Central Europe.

Moschids are enigmatic pecoran ruminants whose phylogeny is still not fully understood. So far we know only little of the family's early evolutionary history and the origin of the modern genus, Moschus. Here we present a comprehensive description of cranial material, including the ear region and the dentition, of fossil moschid material from the Middle Miocene locality Steinheim am Albuch (13.5 Ma; Germany). This study provides the first exhaustive dataset for the cranial osteology of Micromeryx flourensianus, the most likely oldest true moschid. It furthermore reveals the presence of a second, so far undescribed moschid species, we here name Micromeryx? eiselei, in the abundant material from the locality. The two taxa can be clearly distinguished by characters of the skull, the ear region, the dentition, as well as by size. This evidences the sympatric occurrence of two moschid species in the locality Steinheim am Albuch.

Heterochronic evolution explains novel body shape in a Triassic coelacanth from Switzerland.

A bizarre latimeriid coelacanth fish from the Middle Triassic of Switzerland shows skeletal features deviating from the uniform anatomy of coelacanths. The new form is closely related to a modern-looking coelacanth found in the same locality and differences between both are attributed to heterochronic evolution. Most of the modified osteological structures in the new coelacanth have their developmental origin in the skull/trunk interface region in the embryo. Change in the expression of developmental patterning genes, specifically the Pax1/9 genes, may explain a rapid evolution at the origin of the new coelacanth. This species broadens the morphological disparity range within the lineage of these 'living fossils' and exemplifies a case of rapid heterochronic evolution likely trigged by minor changes in gene expression.

A new primate assemblage from La Verrerie de Roches (Middle Eocene, Switzerland).

Primates reached a great abundance and diversity during the Eocene, favored by warm temperatures and by the development of dense forests throughout the Northern Hemisphere. Here we describe new primate material from La Verrerie de Roches, a Middle Eocene karstic infill situated in the Jura Region (Switzerland), consisting of more than 80 dental remains. The primate assemblage from La Verrerie de Roches includes five different taxa. The best represented primate is Necrolemur aff. anadoni, similar in size and overall morphology to Necrolemur anadoni but resembling in some features the younger species Necrolemur antiquus. Microchoerines are also represented by two species of Pseudoloris, P. pyrenaicus and Pseudoloris parvulus, constituting the unique joint record of these two species known up to now. Remains of Adapiformes are limited to one isolated tooth of a large anchomomyin and another tooth belonging to the small adapine Microadapis cf. sciureus. The studied primate association allows assigning La Verrerie de Roches to the Robiacian Land Mammal Age. More specifically, this site can be confidently situated between the MP15 and MP16 reference levels, although the primate assemblage probably indicates some degree of temporal mixing. This is the first record of P. pyrenaicus and a form closely related to N. anadoni out of the Iberian Peninsula. The identification of these microchoerines in Switzerland gives further support to the connection of NE Spain and Central Europe during the Middle Eocene.

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.

Size Variation under Domestication: Conservatism in the inner ear shape of wolves, dogs and dingoes.

A broad sample of wolves, dingoes, and domesticated dogs of different kinds and time periods was used to identify changes in size and shape of the organs of balance and hearing related to domestication and to evaluate the potential utility of uncovered patterns as markers of domestication. Using geometric morphometrics coupled with non-invasive imaging and three-dimensional reconstructions, we exposed and compared complex structures that remain largely conserved. There is no statistically significant difference in the levels of shape variation between prehistoric and modern dogs. Shape variance is slightly higher for the different components of the inner ear in modern dogs than in wolves, but these differences are not significant. Wolves express a significantly greater level of variance in the angle between the lateral and the posterior canal than domestic dog breeds. Wolves have smaller levels of size variation than dogs. In terms of the shape of the semicircular canals, dingoes reflect the mean shape in the context of variation in the sample. This mirrors the condition of feral forms in other organs, in which there is an incomplete return to the characteristics of the ancestor. In general, morphological diversity or disparity in the inner ear is generated by scaling.

Microchoerus hookeri nov. sp., a new late Eocene European microchoerine (Omomyidae, Primates): New insights on the evolution of the genus Microchoerus.

The study of Eocene primates is crucial for understanding the evolutionary steps undergone by the earliest members of our lineage and the relationships between extinct and extant taxa. Recently, the description of new material from Spain has improved knowledge of European Paleogene primates considerably, particularly regarding microchoerines. Here we describe the remains of Microchoerus from Sossís (late Eocene, Northern Spain), consisting of more than 120 specimens and representing the richest sample of Microchoerus from Spain. This primate was first documented in Sossís during the 1960s, on the basis of scarce specimens that were ascribed to Microchoerus erinaceus. However, the studied material clearly differs from M. erinaceus at its type locality, Hordle Cliff, and shows some characters that allow the erection of a new species, Microchoerus hookeri. This new species is characterized by its medium size, moderate enamel wrinkling, generally absent mesoconid and small hypoconulid in the M1 and M2, single paracone in the upper molars and premolars and, particularly, by the lack of mesostyle in most M1 and M2, a trait not observed in any other species of Microchoerus. Some specimens from Eclépens B (late Eocene, Switzerland), determined previously to be Microcherus aff. erinaceus, are also ascribed to M. hookeri. M. hookeri represents the first step of a lineage that differentiated from Necrolemur antiquus and, later, gave rise to several unnamed forms of Microchoerus, such as those from Euzet and Perrière, finally leading to M. erinaceus. This discovery sheds new light on the complex evolutionary scheme of Microchoerus, indicating that it is most probably a paraphyletic group. A detailed revision of the age of the localities containing remains of Microchoerus and the description of the still unpublished material from some European localities, are necessary to clarify the phylogenetic relationships among the members of this microchoerine group.

Prenatal growth stages show the development of the ruminant bony labyrinth and petrosal bone.

Foetuses are a source of scientific information to understand the development and evolution of anatomical structures. The bony labyrinth, surrounding the organ of balance and hearing, is a phylogenetically and ecologically informative structure for which still little concerning growth and shape variability is known in many groups of vertebrates. Except in humans, it is poorly known in many other placentals and its prenatal growth has almost never been studied. Ruminants are a diversified group of placentals and represent an interesting case study to understand the prenatal growth of the ear region. We computed tomography -scanned five cow foetuses and an adult petrosal bone (Bos taurus, Artiodactyla, Mammalia), and describe the bony labyrinth when already ossified. The foetuses encompass the second half of the 9.3-month-long gestation period of the cow. They were sampled at different ontogenetic stages to understand how and when the petrosal bone and bony labyrinth ossify in ruminants. The petrosal bone and bony labyrinth ossify within about 20 days in the fourth month of gestation. The bony labyrinth is already fully ossified at least in the 6th month, while only the cochlea, most of the vestibule and the common crus are already ossified at the beginning of the 4th month. The pars canalicularis of the petrosal thus ossifies at last. The size and volume of the bony labyrinth stay similar from the 6th month (possibly even from the 5th). From the end of the 4th month of gestation, a progressive lengthening of the cochlear aqueduct and endolymphatic sac occurs, culminating in the adult form and partly explaining the larger volume of the later. The inner ear in the cow ossifies quickly during the gestation period, being fully ossified around mid-gestation time, as in humans. The adult size and most of its volume are reached by mid-gestation time while the petrosal bone and skull still grow. A negative ontogenetic allometry between the bony labyrinth and the petrosal bone and skull is thus observed. It matches the evolutionary negative allometry of the structure observed in earlier studies. Few changes occur after ossification is achieved; only open structures (i.e. cochlear aqueduct and endolymphatic sac) continue to grow after birth and reflect size increase of the petrosal bone.

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.

Shape variation and ontogeny of the ruminant bony labyrinth, an example in Tragulidae.

Despite its growing use in anatomical and ecological studies, the morphological variability and ontogenetic development of the bony labyrinth have very rarely been investigated in ruminants. Here we study its morphology in 15 adult and 10 juvenile specimens in the three extant tragulid ruminant genera. Intraspecific and interspecific variability is quantified using morphometric and 3D geometric morphometrics analyses. The bony labyrinth of Tragulus, Hyemoschus, and Moschiola is strikingly different, clustering in clearly different morphospaces despite similar ecological adaptations. Although the bony labyrinths within two species of the same genus cannot be distinguished from each other based on the chosen semi-landmarks, discrete interspecific differences exist. We were able to show for the first time that an artiodactyl mammal in a late fetal stage possesses an almost fully formed bony labyrinth similar to that of adults. No significant change either occurs in size or morphology after ossification of the petrosal bone. Some intraspecific variation is observed on the shape of the lateral semi-circular canal, the size and shape of the common crus, the coil of the cochlea or the stapedial ratio. Variable structures are expected to be highly informative characters for a large cladistic analysis. They can be used for phylogenetic studies in ruminants. Incorporating juvenile specimens in studies is not problematic, as they fall within the morphological range of adults.

Testing for Depéret's Rule (Body Size Increase) in Mammals using Combined Extinct and Extant Data.

Whether or not evolutionary lineages in general show a tendency to increase in body size has often been discussed. This tendency has been dubbed "Cope's rule" but because Cope never hypothesized it, we suggest renaming it after Depéret, who formulated it clearly in 1907. Depéret's rule has traditionally been studied using fossil data, but more recently a number of studies have used present-day species. While several paleontological studies of Cenozoic placental mammals have found support for increasing body size, most studies of extant placentals have failed to detect such a trend. Here, we present a method to combine information from present-day species with fossil data in a Bayesian phylogenetic framework. We apply the method to body mass estimates of a large number of extant and extinct mammal species, and find strong support for Depéret's rule. The tendency for size increase appears to be driven not by evolution toward larger size in established species, but by processes related to the emergence of new species. Our analysis shows that complementary data from extant and extinct species can greatly improve inference of macroevolutionary processes.

Primate tarsal bones from Egerkingen, Switzerland, attributable to the middle Eocene adapiform Caenopithecus lemuroides.

The middle Eocene species Caenopithecus lemuroides, known solely from the Egerkingen fissure fillings in Switzerland, was the first Paleogene fossil primate to be correctly identified as such (by Ludwig Rütimeyer in 1862), but has long been represented only by fragmentary mandibular and maxillary remains. More recent discoveries of adapiform fossils in other parts of the world have revealed Caenopithecus to be a biogeographic enigma, as it is potentially more closely related to Eocene adapiforms from Africa, Asia, and North America than it is to any known European forms. More anatomical evidence is needed, however, to provide robust tests of such phylogenetic hypotheses. Here we describe and analyze the first postcranial remains that can be attributed to C. lemuroides-an astragalus and three calcanei held in the collections of the Naturhistorisches Museum Basel that were likely recovered from Egerkingen over a century ago. Qualitative and multivariate morphometric analyses of these elements suggest that C. lemuroides was even more loris-like than European adapines such as Adapis and Leptadapis, and was not simply an adapine with an aberrant dentition. The astragalus of Caenopithecus is similar to that of younger Afradapis from the late Eocene of Egypt, and parsimony and Bayesian phylogenetic analyses that include the new tarsal data strongly support the placement of Afradapis and Caenopithecus as sister taxa to the exclusion of all other known adapiforms, thus implying that dispersal between Europe and Africa occurred during the middle Eocene. The new tarsal evidence, combined with previously known craniodental fossils, allows us to reconstruct C. lemuroides as having been an arboreal and highly folivorous 1.5-2.5 kg primate that likely moved slowly and deliberately with little or no capacity for acrobatic leaping, presumably maintaining consistent powerful grasps on branches in both above-branch and inverted postures.