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.

Classifying fossil Darwin wasps (Hymenoptera: Ichneumonidae) with geometric morphometrics of fore wings.

Linking fossil species to the extant diversity is often a difficult task, and the correct interpretation of character evidence is crucial for assessing their taxonomic placement. Here, we make use of geometric morphometrics of fore wings to help classify five fossil Darwin wasps from the Early Eocene Fur Formation in Denmark into subfamilies and often tribes. We compile a reference dataset with 342 fore wings of nine extant subfamilies and nine relevant fossil species. Since geometric morphometrics was mostly ignored in the past in Darwin wasp classification, the dataset is first used to examine differences and similarities in wing venation among subfamilies. In a next step, we used the reference dataset to inform the classification of the fossil species, which resulted in the description of one new genus and five new species, Crusopimpla weltii sp. nov., Ebriosa flava gen. et sp. nov., Entypoma? duergari sp. nov., Lathrolestes? zlatorog sp. nov., and Triclistus bibori sp. nov., in four different subfamilies. Carefully assessing data quality, we show that the fore wing venation of fossil Darwin wasps is surprisingly suitable to assign them to a subfamily or even lower taxonomic level, especially when used in conjunction with characters from other parts of the body to narrow down a candidate set of potential subfamilies and tribes. Our results not only demonstrate a fast and useful approach to inform fossil classification but provide a basis for future investigations into evolutionary changes in fore wings of ichneumonids. The high informativeness of wing venation for classification furthermore could be harvested for phylogenetic analyses, which are otherwise often hampered by homoplasy in this parasitoid wasp family.

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.

A new gigantic carnivore (Carnivora, Amphicyonidae) from the late middle Miocene of France.

Serravallian terrestrial vertebrates are very uncommon in the northern margin of the Pyrenean Mountains. A mandible of a new large sized amphicyonid (ca. 200 kg) is here described from the marine deposits of Sallepisse (12.8-12.0 Mya). Despite that this new taxon is close in size to some European amphicyonids from the Miocene (e.g., Amphicyon, Megamphicyon, and Magericyon), the unique morphology of its p4, unknown in this clade, allows the erection of the new genus Tartarocyon cazanavei nov. gen. & sp. This taxon may be derived from a Cynelos-type amphicyonine. The description of this new taxon highlights the erosion of the ecological and morphological diversity of the Amphicyonidae in response to well-known Miocene events (i.e., Proboscidean Datum Event, Middle Miocene Climatic Transition, Vallesian Crisis).

Size and shape of the semicircular canal of the inner ear: A new marker of pig domestication?

Domestication has led to many changes in domestic animal biology, including their anatomy. The shape of the inner ear, part of the mammalian ear, has been found particularly relevant for discriminating domesticated species, their hybrids or differentiating the wild and domestic populations of a single species. Here we assessed the use of the size and shape of the semicircular canals (SCC) of the inner ear as a marker of pig domestication. We studied a total of 63 petrosal bones belonging to wild boar (Sus scrofa, two populations) and domestic pigs (extensively and intensively reared specimens) that were µCT-scanned and from which the size and the shape of the inner ear were quantified through geometric morphometrics, analyzing the 3D coordinates of 6 landmarks and 60 sliding semilandmarks localized on the SCC and the common crus. The domestic pigs have larger SCC than the wild boar from which they also strongly differ in shape (correct cross validation of 95.5%, confidence interval: 92.3%-98.1%). Strong shape differences were detected between the two populations of wild boar, as well as a sexual size dimorphism. All together the results highlight the taxonomic discriminant power of the SCC of the inner ear shape, and its relevance for domestication studies.

Ruminants reveal Eocene Asiatic palaeobiogeographical provinces as the origin of diachronous mammalian Oligocene dispersals into Europe.

Faunal provincialism between the North and South parts of Eastern Asia is shown to have been in place since the late Eocene. This provincialism structured the mammalian dispersals across Eurasia for millions of years and provides insights into both palaeonvironments and palaeoclimate zonation. In addition, this study reveals the oldest record of a crown ruminant (Iberomeryx from Shinao, China). Ecologically, as well as economically, ruminant artiodactyls are one of the most important large mammal groups today. The revision of the ruminants from the Shinao Formation, from the Caijiachong marls and Xiaerhete, resulted in two new taxa and shows that the different provinces were populated by distinct taxa living in different environments, dominated by the monsoon in the South and drier conditions in the North. Evaluating this result in a Eurasian context demonstrates that the dispersals from Asia to Europe was complex. These results confirm that there were at least two dispersal events, distinct in space and time: the Grande-Coupure from Northern and Central Asia along the North ca. 34 Mya and the Bachitherium dispersal event from the Southern province along a southerly route ca. 31 Mya.

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.

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).

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.

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.

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.

The European ruminants during the "Microbunodon Event" (MP28, Latest Oligocene): impact of climate changes and faunal event on the ruminant evolution.

The Earth already experienced numerous episodes of global warming and cooling. One of the latest impressive events of temperature rising was the Late Oligocene Warming that occurred around 25 Mya. An increase of the marine temperature of 2 to 4°C has been observed in a short time interval. In Europe, this major climatic event can be correlated to the continental faunal turnover "Microbunodon Event". This event is marked by a huge faunal turnover (40% of the ungulate fauna during the first 500k years) and environmental changes. Drier conditions associated to the appearance of the seasonality lead to new environmental conditions dominated by wooded savannahs. This is correlated to a major arrival of Asiatic immigrants. Moreover, from a homogenous fauna during the main part of the Oligocene, local climatic variations between the European Western coast and the more central Europe could have provided faunal regionalism during the latest Oligocene and earliest Miocene. Considering the ruminants, this event is the major ever known for this group in Europe. A total renewal at the family level occurred. Thanks to a precise stratigraphic succession, major evolutionary elements are highlighted. Typical Oligocene species, mainly Tragulina, were adapted to wooded environments and were leaves/fruits eaters. They disappeared at the end of MP27 or the early MP28. This corresponds to the appearance of the Asiatic immigrants. The Tragulina (Lophiomerycidae, Bachitheriidae) and stem Pecora gave way to more derived stem and maybe crown Pecora (e.g. "Amphitragulus", Babameryx, Dremotherium). These newcomers were adapted to more open environments and mixed feeding. The disappearance of the Tragulina is probably linked to environmental and vegetation changes, and competition. They give way to more derived ruminants having a more efficient metabolism in drier conditions and a better assimilation of less energetic food.