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.

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.

Correction: Eocene metatherians from Anatolia illuminate the assembly of an island fauna during Deep Time.

[This corrects the article DOI: 10.1371/journal.pone.0206181.].

Eocene metatherians from Anatolia illuminate the assembly of an island fauna during Deep Time.

Island biotas have disproportionately influenced the history and development of evolutionary biology, but understanding their genesis and evolution across geological timescales has been hindered by a poor fossil record. Here we augment the insular Eocene (~43 Ma) mammalian fauna known from the Pontide terrane of central Anatolia by describing two new metatherian taxa (stem marsupials) from the Lülük Member of the Uzunçarsidere Formation in the Orhaniye Basin. Geological and paleontological data indicate that the Pontide terrane was an island on the northern margin of Neotethys during the middle Eocene. Reflecting its geodynamic context in a region of active tectonic convergence, the Eocene Pontide terrane hosted a unique combination of Laurasian and Gondwanan mammals, including an anachronistic radiation of pleuraspidotheriids (archaic ungulates) that went extinct on the European mainland ~13 Ma earlier. Most of the mammalian clades occupying the Pontide terrane colonized it by dispersal across marine barriers rather than being stranded there through vicariance. Endemic radiations of pleuraspidotheriid ungulates and polydolopimorphian metatherians on the Pontide terrane reveal that in situ diversification was an important factor contributing to faunal assembly and evolution. The insular fauna that arose on the Pontide terrane is highly analogous to that of modern Sulawesi, which evolved under strikingly similar geological conditions. Illustrating the ephemeral nature of insular biotas across macroevolutionary timescales, the demise of the Pontide fauna coincided with paleogeographic changes enabling more cosmopolitan taxa to reach it for the first time. The high level of endemism shown by the mammalian fauna of the Uzunçarsidere Formation eliminates the Pontide terrane as a potential early Eocene dispersal corridor between western Europe and India.

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.

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.

New Early Cenozoic ghost shrimps (Decapoda, Axiidea, Callianassidae) from Pakistan and their palaeobiogeographic implications.

A new set of Paleocene and Eocene decapod crustaceans is described from the Kirthar Range of Pakistan. Two new ghost shrimps (Crustacea, Decapoda, Callianassidae) are described: Neocallichirus khadroensis Hyzný & Charbonnier, n. sp. from the Paleocene (Danian, Khadro Formation) of Gawar Band, Ranikot District, and Neocallichirus lakhraensis Hyzný & Charbonnier, n. sp. from the Early Eocene (Ypresian, Lakhra Formation) of Rbod Nala, Jhirak District. Both new species exhibit chelipeds which are morphologically surprisingly close to extant Neocallichirus karumba (Poore & Griffin, 1979) from the Indo-West Pacific. A group of species sharing this same cheliped morphology is provisionally called the "karumba group" based on Neocallichirus karumba, best documented species. The "karumba group" encompasses seven fossil species: the two new Pakistani species, Neocallichirus tuberculatus (Lorenthey in Lorenthey & Beurlen, 1929) n. comb. from the Eocene of Hungary, Neocallichirus borensis Beschin, De Angeli, Checchi & Mietto, 2006 from the Eocene of Italy, Neocallichirus birmanicus (Noetling, 1901) n. comb. from the Miocene of Myanmar, Neocallichirus dijki (Martin, 1883) from the Miocene of Java and Philippines, and the subfossil Neocallichirus maximus (A. Milne-Edwards, 1870) from Thailand. Based upon the extant and fossil occurrences, it is difficult to reconstruct migration pattern of the "karumba group". For now, it can be concluded, that at the genus level, a relative homogeneity of the ghost shrimps is observed between the Eastern and the Western Tethyan regions, as already suggested by Merle et al. (2014) for the assemblage of volutid gastropods from the Lakhra Formation.

Volutidae (Mollusca: Gastropoda) of the Lakhra Formation (Earliest Eocene, Sindh, Pakistan): systematics, biostratigraphy and paleobiogeography.

The paleobiodiversity of the Volutidae (Mollusca: Gastropoda) of the Ranikot Group (Sindh, Pakistan) and particularly of the Lakhra Formation (SBZ 5 biozone, Earliest Eocene), is reconsidered on the basis of new material collected during recent field trips. Ten new species are described (Mitreola brohii sp. nov., Lyrischapa vredenburgi sp. nov., L. brevispira sp. nov., Athleta (Volutopupa) citharopsis sp. nov., A. (Volutocorbis) lasharii sp. nov., Volutilithes welcommei sp. nov., V. sindhiensis sp. nov., Pseudaulicina coxi sp. nov., Sindhiluta lakhraensis sp. nov. and Pakiluta solangii sp. nov.) and one species is in open nomenclature (Lyria sp.). Three new genera are described: Lyriopsis gen. nov. [Volutinae, ?Lyriini, type species: Lyriopsis cossmanni (Vredenburg, 1923)], Sindhiluta gen. nov. [Volutilithinae, type species: Sindhiluta lakhraensis n. sp.] and Pakiluta gen. nov. [?Volutodermatinae, type species: Pakiluta solangii n. sp.]. Two new combinations are proposed: Lyriopsis cossmanni (Vredenburg, 1923) comb. nov. and Athleta (Volutopupa) intercrenatus (Cossmann & Pissarro, 1909) comb. nov. Lectotypes are designated for Lyria cossmanni Vredenburg, 1923, L. feddeni Vredenburg, 1923, Volutospina noetlingi Cossmann & Pissarro, 1909, V. intercrenata Cossmann & Pissarro, 1909 and Athleta (Volutocorbis) victoriae Vredenburg, 1923. With 21 species, this volutid fauna is the most diverse recorded from the Tethys Ocean during Earliest Eocene time. The assemblage is characterized by a strong turnover marked by regional speciation and the appearance of many western Tethyan invaders. Although at the species level, the assemblage documents a strong provincialism, at the genus level, the high number of shared genera between Eastern Tethyan and Old World Tethyan realms begins a phase of long-term homogeneity of volutid assemblages from the Tethyan paleobiogeographic province.

First Clarkforkian equivalent Land Mammal Age in the latest Paleocene basal Sparnacian facies of Europe: fauna, flora, paleoenvironment and (bio)stratigraphy.

The Paleocene-Eocene Thermal Maximum (PETM) is correlated with the first occurrences of earliest modern mammals in the Northern Hemisphere. The latest Paleocene Clarkforkian North American Land Mammal Age, that has yielded rodents and carnivorans, is the only exception to this rule. However, until now no pre-PETM localities have yielded modern mammals in Europe or Asia. We report the first Clarkforkian equivalent Land Mammal Age in the latest Paleocene deposits of the basal Sparnacian facies at Rivecourt, in the north-central part of the Paris Basin. The new terrestrial vertebrate and macroflora assemblages are analyzed through a multidisciplinary study including sedimentologic, stratigraphic, isotopic, and palynological aspects in order to reconstruct the paleoenvironment and to evaluate biochronologic and paleogeographic implications. The mammals are moderately diverse and not abundant, contrary to turtles and champsosaurs. The macroflora is exceptional in preservation and diversity with numerous angiosperms represented by flowers, fruits, seeds and wood preserved as lignite material, revealing an abundance of Arecaceae, Betulaceae, Icacinaceae, Menispermaceae, Vitaceae and probably Cornaceae. Results indicate a Late Paleocene age based on carbon isotope data, palynology and vertebrate occurrences such as the choristoderan Champsosaurus, the arctocyonid Arctocyon, and the plesiadapid Plesiadapis tricuspidens. However, several mammal species compare better with the earliest Eocene. Among these, the particular louisinid Teilhardimys musculus, also recorded from the latest Paleocene of the Spanish Pyrenees, suggests a younger age than the typical MP6 reference level. Nevertheless, the most important aspect of the Rivecourt fauna is the presence of dental remains of a rodent and a "miacid" carnivoran, attesting to the presence of two modern mammalian orders in the latest Paleocene of Europe. Interestingly, these two groups are also the only modern groups recorded from the latest Paleocene of North America, making Rivecourt the first direct equivalent to the Clarkforkian Land Mammal Age outside of North America.

Listriodon guptai Pilgrim, 1926 (Mammalia, Suidae) from the early Miocene of the Bugti Hills, Balochistan, Pakistan: new insights into early Listriodontinae evolution and biogeography.

New dental remains of listriodont suids are described from the lower member of the early to middle Miocene Vihowa Formation of the Bugti Hills, Pakistan. The material is homogeneous in terms of morphology and dimensions and referred as a whole to Listriodon guptai Pilgrim, 1926. This species is also mentioned in coeval deposits of the Zinda Pir Dome, Pakistan, dating back to ca. 19 Ma. The early occurrence of an advanced listriodont in Pakistan constrains the age of acquisition of several characters correlated to lophodonty within Listriodontini, and raises major questions about the early history of the Old World Listriodontinae. Strong morphological similarity between Listriodon guptai and the African species Listriodon akatikubas found in the late early Miocene of Maboko (Kenya, ca. 16.5 Ma) suggests that this latter is most probably a migrant originating from Asia.

Middle-Eocene artiodactyls from Shanghuang (Jiangsu Province, Coastal China) and the diversity of basal dichobunoids in Asia.

A new assemblage of basal dichobunoid artiodactyls from the middle-Eocene Shanghuang fissure fillings includes the diacodexeid Jiangsudon shanghuangensis gen. and sp. nov., a new species of the lantianine dichobunoid Elaschitotherium, Elaschitotherium crepaturus sp. nov., and an indeterminate suoid which is presently the earliest record of this clade. Diacodexeids are also represented by two forms provisionally referred to cf. Diacodexis sp. and to an indeterminate Diacodexeidae, respectively. The occurrence of diacodexeids in Shanghuang contrasts with the early and earliest middle-Eocene chronological range of the family in Europe and North America and suggests that the stratigraphic range of the family in Asia extends up to the middle Eocene. This may reflect particular habitats in coastal China that may have been relatively stable during the early and middle Eocene, thus preserving forest-dwelling artiodactyls that became extinct in the other Holarctic regions. Compared to other supposedly coeval North American, European, and Asian faunas, the Shanghuang mammalian assemblage is most similar to early Uintan faunas of North America but is also remarkable in recording forms close to taxa that are characteristic of the Wasatchian and Bridgerian North American Land Mammal Ages. The Irdinmanhan age of the Shanghuang fauna is supported by the mammalian assemblage recovered from the fissure D, but an Arshantan age cannot be completely ruled out at this point. Although the Shanghuang assemblage is biased towards preservation of small components of the mammalian fauna, the Shanghuang fauna provide an important and unique window into the Eocene diversity and early evolution of cetartiodactyls in eastern Asia.

Artiodactyls from the Pondaung Formation (Myanmar): new data and reevaluation of the South Asian Faunal Province during the Middle Eocene.

Although Asia is thought to have played a critical role in the radiation of artiodactyls, the fossil record of stem selenodonts ("dichobunoids") remains dramatically poor in tropical Asian regions. In this study, we report a new dichobunid genus and species Cadutherium kyaukmagyii and a new basal ruminant genus and species Irrawadymeryx pondaungi, from the late Middle Eocene Pondaung Formation, Central Myanmar. Although the scarcity of the present material prevents any attempts to investigate the phylogenetic relationships of Cadutherium with contemporaneous forms from other Holarctic landmasses, this new form shed new light on the diversity of these small rabbit-like ungulates during a key period of their evolutionary history. Reexamination of the small-bodied artiodactyls from Pondaung leads us to propose new identifications of certain published specimens and, in turn, to investigate the temporal and geographic distribution of taxa recognized in the Pondaung Formation. Although fragmentary, these potential new taxa reveal an unsuspected diversity of small forms among artiodactyls of Pondaung. This addition to the Eocene record of dichobunoids and early ruminants provides further insight in the diversity of dental patterns among small artiodactyls from the Pondaung Formation and attests to the antiquity of these groups in Southeast Asia.

Eocene bunoselenodont Artiodactyla from southern Thailand and the early evolution of Ruminantia in South Asia.

Although Asia is thought to have played a critical role in the basal radiation of Ruminantia, the fossil record of early selenodont artiodactyls remains poorly documented in this region. Dental remains of a new bunoselenodont artiodactyl are described from the late Eocene of Krabi, southern Thailand. This new form, Krabitherium waileki gen. et sp. nov, is tentatively referred to the Tragulidae (Ruminantia) on the basis of several dental features, including a weak Tragulus fold and the presence of a deep groove on the anterior face of the entoconid. Although this new form is suggestive of the enigmatic? Gelocus gajensis Pilgrim 1912 from the "base of the Gaj" (lower Chitarwata Formation) of the Bugti Hills (Central Pakistan), K. waileki most likely represents an early representative of a relatively bunodont group of tragulids that includes the genus Dorcabune, known from the Miocene of south Asia. This addition to the Eocene record of early ruminants attests to the antiquity of the group in Southeast Asia and lends support to the hypothesis that the Tragulidae represents one of the first offshoots in the evolutionary history of Ruminantia.

New remains of the enigmatic cetartiodactyl Bugtitherium grandincisivum Pilgrim, 1908, from the upper Oligocene of the Bugti Hills (Balochistan, Pakistan).

Newly discovered fossil material of the enigmatic cetartiodactyl Bugtitherium grandincisivum from the upper Oligocene of the Bugti Member of the Chitarwata Formation in the Bugti Hills (Balochistan, Pakistan) is reported. These new specimens consist of two fragmentary muzzles (one preserving the first incisors and belonging to a juvenile) and a fragmentary right mandible with m3. The morphologies of the anterior dentition and m3 provided by these new specimens confirm the validity of the genus Bugtitherium and advocate probable anthracotheriid affinity for the genus rather than entelodontid or suoid affinities, but do not definitively close the debate about Bugtitherium's familial affinities within Cetartiodactyla. Although still poorly documented, this large-sized anthracotheriid-like cetartiodactyl is a possible key form for understanding the early evolution of hippos, and, in turn, the ancestry of whales, because of both its morphological similarities with hippos and primitive Paleogene whales and its Tethysian distribution.

Laonastes and the "Lazarus effect" in recent mammals.

The living Laotian rodent Laonastes aenigmamus, first described in early 2005, has been interpreted as the sole member of the new family Laonastidae on the basis of its distinctive morphology and apparent phylogenetic isolation from other living rodents. Here we show that Laonastes is actually a surviving member of the otherwise extinct rodent family Diatomyidae, known from early Oligocene to late Miocene sites in Pakistan, India, Thailand, China, and Japan. Laonastes is a particularly striking example of the "Lazarus effect" in Recent mammals, whereby a taxon that was formerly thought to be extinct is rediscovered in the extant biota, in this case after a temporal gap of roughly 11 million years.

Anthropoid primates from the Oligocene of Pakistan (Bugti Hills): data on early anthropoid evolution and biogeography.

Asian tarsiid and sivaladapid primates maintained relictual distributions in southern Asia long after the extirpation of their close Holarctic relatives near the Eocene-Oligocene boundary. We report here the discovery of amphipithecid and eosimiid primates from Oligocene coastal deposits in Pakistan that demonstrate that stem anthropoids also survived in southern Asia beyond the climatic deterioration that characterized the Eocene-Oligocene transition. These fossils provide data on temporal and paleobiogeographic aspects of early anthropoid evolution and significantly expand the record of stem anthropoid evolution in the Paleogene of South Asia.