Resolving the evolution of the mammalian middle ear using Bayesian inference

Background

The minute, finely-tuned ear ossicles of mammals arose through a spectacular evolutionary transformation from their origins as a load-bearing jaw joint. This involved detachment from the postdentary trough of the mandible, and final separation from the dentary through resorption of Meckel’s cartilage. Recent parsimony analyses of modern and fossil mammals imply up to seven independent postdentary trough losses or even reversals, which is unexpected given the complexity of these transformations. Here we employ the first model-based, probabilistic analysis of the evolution of the definitive mammalian middle ear, supported by virtual 3D erosion simulations to assess for potential fossil preservation artifacts.

Results

Our results support a simple, biologically plausible scenario without reversals. The middle ear bones detach from the postdentary trough only twice among mammals, once each in the ancestors of therians and monotremes. Disappearance of Meckel’s cartilage occurred independently in numerous lineages from the Late Jurassic to the Late Cretaceous. This final separation is recapitulated during early development of extant mammals, while the earlier-occurring disappearance of a postdentary trough is not.

Conclusions

Our results therefore suggest a developmentally congruent and directional two-step scenario, in which the parallel uncoupling of the auditory and feeding systems in northern and southern hemisphere mammals underpinned further specialization in both lineages. Until ~168 Ma, all known mammals retained attached middle ear bones, yet all groups that diversified from ~163 Ma onwards had lost the postdentary trough, emphasizing the adaptive significance of this transformation.

     

Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear

The middle ear bones of Mesozoic mammals are rarely preserved as fossils and the morphology of these ossicles in the earliest mammals remains poorly known. Here, we report the stapes and incus of the euharamiyidan Arboroharamiya from the lower Upper Jurassic (～160 Ma) of northern China, which represent the earliest known mammalian middle ear ossicles. Both bones are miniscule in relation to those in non‐mammalian cynodonts. The skull length/stapedial footplate diameter ratio is estimated as 51.74 and the stapes length as the percentage of the skull length is 4%; both numbers fall into the stapes size ranges of mammals. The stapes is “rod‐like” and has a large stapedial foramen. It is unique among mammaliaforms in having a distinct posterior process that is interpreted as for insertion of the stapedius muscle and homologized to the ossified proximal (stapedial) end of the interhyal, on which the stapedius muscle attached. The incus differs from the quadrate of non‐mammalian cynodonts such as morganucodontids in having small size and a slim short process. Along with lack of the postdentary trough and Meckelian groove on the medial surface of the dentary, the ossicles suggest development of the definitive mammalian middle ear (DMME) in Arboroharamiya. Among various higher‐level phylogenetic hypotheses of mammals, the one we preferred places “haramiyidans” within Mammalia. Given this phylogeny, development of the DMME took place once in the allotherian clade containing euharamiyidans and multituberculates, probably independent to those of monotremes and therians. Thus, the DMME has evolved at least three times independently in mammals. Alternative hypothesis that placed “haramiyidans” outside of Mammalia would require independent acquisition of the DMME in multituberculates and euharamiyidans as well as parallel evolution of numerous derived similarities in the dentition, occlusion pattern, mandibles, cranium, and postcranium between the two groups and between “haramiyidans” and other mammals. J. Morphol. 279:441–457, 2018. © 2016 Wiley Periodicals, Inc.     

Mammalian development does not recapitulate suspected key transformations in the evolutionary detachment of the mammalian middle ear

The ectotympanic, malleus and incus of the developing mammalian middle ear (ME) are initially attached to the dentary via Meckel''s cartilage, betraying their origins from the primary jaw joint of land vertebrates. This recapitulation has prompted mostly unquantified suggestions that several suspected—but similarly unquantified—key evolutionary transformations leading to the mammalian ME are recapitulated in development, through negative allometry and posterior/medial displacement of ME bones relative to the jaw joint. Here we show, using µCT reconstructions, that neither allometric nor topological change is quantifiable in the pre-detachment ME development of six marsupials and two monotremes. Also, differential ME positioning in the two monotreme species is not recapitulated. This challenges the developmental prerequisites of widely cited evolutionary scenarios of definitive mammalian middle ear (DMME) evolution, highlighting the requirement for further fossil evidence to test these hypotheses. Possible association between rear molar eruption, full ME ossification and ME detachment in marsupials suggests functional divergence between dentary and ME as a trigger for developmental, and possibly also evolutionary, ME detachment. The stable positioning of the dentary and ME supports suggestions that a ‘partial mammalian middle ear’ as found in many mammaliaforms—probably with a cartilaginous Meckel''s cartilage—represents the only developmentally plausible evolutionary DMME precursor.     

中国中生代哺乳动物研究进展

迄今为止,中国已知的中生代哺乳动物共有26属29种(包括3个未定种),时代分布从早侏罗世至晚白垩世。在中国新近发现的中生代哺乳动物中,除少数几种材料比较零星之外,大多数都有保存很好的头骨和骨架为代表。它们提供了认识哺乳动物高阶元之间的系统发育关系以及早期演化过程中特征转变的重要信息。过去几年中发现的中生代哺乳动物多数产于热河生物群中。这些化石代表了不同的哺乳动物大类,同时显示了在个体大小、运动姿态以及食性方面的较高的分异。多方面的分异确保了它们在同一个生态系统中能够占据不同的生态位。频繁的火山活动被认为是辽宁西部地区动物大量死亡的主要原因。像巨爬兽(Repenomamus giganticus)一样以睡眠姿势保存的标本,很可能意味着随火山喷发释放出的有毒气体参与造成了这样的灾难。     

A new spalacolestine mammal from the Early Cretaceous Jehol Biota and implications for the morphology,phylogeny, and palaeobiology of Laurasian ‘symmetrodontans’

‘Symmetrodontans’ are extinct mammals characterized by having a reversed‐triangle molar pattern in which three main cusps define a triangular molar crown. This dental morpholgy has been regarded as being intermediate between the ‘triconodont’ tooth and the tribosphenic pattern characterizing therians; it is a key feature in taxonomy of Mesozoic mammals and one to understand mammalian evolution and palaeobiology. Here we report a new genus and species of ‘symmetrodontan’ mammal, Lactodens sheni, from the Early Cretaceous Jehol Biota, represented by a partial skeleton with dentary and upper and lower teeth with dental morphologies well‐preserved. The new species has a dental formula of three upper incisors, one canine, three premolars, and six molars/three lower incisors, one canine, five premolars and six lower molars, double‐rooted canines, extremely low‐crowned and transversely thin premolars, and acute angled molars. The dental morphologies of molars and peculiar deciduous premolars are similar to those of Spalacolestes from North America. The associated upper and lower dentitions from one individual animal helped to clarify tooth identification of some spalacotheriids represented only by fragmentary material. Phylogenetic analyses indicate a close relationship of the new species to North American spalacolestines and faunal interchanges between Eurasia and North America, thus supporting the notion that small‐bodied spalacotheriids were diverse and had a pan‐Laurasian distribution during the Early Cretaceous. Absence of the Meckelian groove suggests acquisition of the definitive mammalian middle ear in spalacolestines, and deciduous canines and premolars in the slim and extremely long dentary imply a faunivorous diet.     

Chondroid bone and secondary cartilage contribute to apical dentary growth in juvenile Atlantic salmon

The microstructure and tissue composition of the dentary bone in Atlantic salmon salmo salar parr were examined using a variety of histological and whole‐mount techniques. Proximally, the dentary is composed of typical cellular lamellar bone with Sharpey's fibres extending dorsally, proximally and ventrally. Meckel's cartilage is located medially through the entire length of the dentary, and degrades distally resulting in a short transitional zone between hyaline cartilage and connective tissue. At the distal tip of the dentary, isogenic clusters of chondrocytes of periosteal origin were observed secreting small amounts of pericellular cartilage matrix within the bone matrix. These characteristics are highly indicative of secondary chondrogenesis, and suggest that the apical part of the dentary bone in Atlantic salmon does not grow via 'pure' intramembranous ossification, but rather via a modified mode of periosteal ossification involving secondary cartilage and chondroid bone. Furthermore, the unusual mode of gender‐related dentary growth (kype formation) in adult male Atlantic salmon could be the continuation of a general mode of salmonid apical dentary growth.     

Water lilies and scarabs: faithful partners for 100 million years?

Night-flowering water lilies (Nymphaeaceae) in South America are pollinated by Cyclocephala scarab beetles (Scarabaeidae: Cyclocephalini) in a specialized relationship involving synchronized flowering movements, strong floral scent, food tissues, and heat-producing flowers. We report that a similar and closely related association exists in West Africa between Nymphaea lotus L. and Ruteloryctes morio Fabricius (Cyclocephalini). This finding strongly supports a late Early Cretaceous origin of a symbiosis between the night-flowering water lilies and pollinating Cyclocephalini beetles. We believe that this is the first unambiguous evidence of a plant-pollinator relationship of this age.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 539–543.     

Size matters: the (negative) allometry of copulatory duration in mammals

The amount of time taken to copulate varies enormously among mammals. Because copulation likely exposes animals to an increased risk of predation, and uses time and energy that could be spent on foraging, smaller mammals (which are vulnerable to more predators and have a shorter time-to-starvation than larger mammals) should spend less time copulating than do larger mammals. Furthermore, if extended copulation reflects competition among males, then the duration of mating (after correction for body size) should be greater in mammals in which females mate with more than one male. We tested these predictions using comparative data from 113 mammalian species in 85 genera, 40 families, and 14 orders, while controlling for the effect of phylogeny. We found: (1) the relationship between duration of copulation and body size to be negative, not positive; (2) no relationship with inferred multiple mating by females (based upon relative testes mass). We suggest that small mammals may find the sustained maneuvering and body positioning of copulation easier than do large mammals. This hypothesis is supported by an apparently isometric relationship between duration of copulation and ratio of power to mass.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 185–193.     

Modulated Expression of Type X Collagen in the Meckel's Cartilage with Different Developmental Fates

Mammalian Meckel's cartilage undergoes regionally diverse histodifferentiation: the caudal end of Meckel's cartilage extends to the developing ear and gives rise to malleus and incus through endochondral ossification while its major distal region differentiates into sphenomandibular ligament and the anterior ligament of the malleus tympanic plate through fibrous transformation. Since the entire Meckel's cartilage develops up to chondrocyte hypertrophy, the regional extracellular matrix components in the hypertrophic Meckel's cartilage may differ in association with the diverse developmental fates. In this project, the expressions of cartilage collagens were investigated in developing rat Meckel's cartilage and particular interest was given to type X collagen. A cDNA, HP114, encoding the NC1 domain of rat α1(X) collagen was cloned, and a synthetic peptide based on the sequence deduced from HP114 was used to generate a monospecific antibody. In situ hybridization of newborn rat condylar and angular cartilages undergoing endochondral ossification showed restricted labeling with the α1(X) collagen probe in the hypertrophic chondrocyte layer. In contrast, the α1(X) collagen probe totally failed to label the major distal portion of Meckel's cartilage even in the hypertrophic cartilage zone. Immunohistochemistry using the anti-type X collagen monospecific antibody consistently failed to recognize the epitope in the corresponding portion of Meckel's cartilage throughout the experimental periods of gestational Day 17, newborn, and Postnatal Day 7, while the strictly localized positive staining was found in the posterior part of Meckel's cartilage which gave rise to malleus and incus. Since major cartilage collagens type II and type IX were found to be present throughout Meckel's cartilage, we postulate that the regulatory molecular mechanism of type X collagen expression may be closely associated with the developmental fates of fibrous transformation and endochondral ossification in mammalian Meckel's cartilage.     

The adaptive significance of coloration in lagomorphs

Lagomorph pelage coloration was matched to habitat type, geographical region, altitude and behaviour to explore the adaptive significance of coloration patterns in this little-studied order of mammals. Analyses were conducted with and without taking phylogeny into account. The former analyses were based on a weighted, phylogenetic supertree for all extant species of lagomorphs that we constructed using morphological and molecular data from 146 papers in the literature. Although our analyses represent an initial, somewhat crude investigation, several clear trends are evident. First, overall body coloration across lagomorphs tends to match the background as shown for pale and red coloration and perhaps seasonal pelage change. The case for countershading being a method of concealment is far less strong. Second, ear tips appear to have a communicative role since they are conspicuous in many different habitats. Third, hypotheses for tail tips having a communicative role, for extremities being dark for physiological reasons, and for Gloger's rule received only partial support.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79, 309–328.     

Evolutionary analysis of the middle and inner ear of Late Jurassic multituberculates

We describe three previously unreported specimens of petrosal bones of paulchoffatiid multituberculate mammals, collected from strata of Late Jurassic age in the Guimarota lignite mine of Leiria, west-central Portugal. The new fossils allow correction, supplementation, and confirmation of anatomical details, thus refining knowledge of general adaptation in the ear region among Jurassic multituberculates. Virtually all observed characters in the paulchoffatiid otic region are primitive relative to homologous features seen among Late Cretaceous and younger representatives of the Multituberculata; we recognize few unique otic specializations in paulchoffatiids that would preclude ancestry to later multituberculates. The plesiomorphic nature of paulchoffatiid ear regions provides no evidence in support of the hypothesis of a special, sister-group relationship between multituberculates and Late Cretaceous/Cenozoic marsupials plus placentals. Used in isolation, objective evidence derived from paulchoffatiid ear regions is consistent with interpretation of multituberculate divergence from other mammals predating the stem to living monotremes and postdating the stem to extinct morganucodontids. More broadly based comparative studies among Mesozoic mammals, however, suggest that independent acquisition of similarly advanced mammalian features was a pervasive theme among evolutionary histories of early mammals, probably including multituberculates. Although the phylogenetic position of multituberculates relative to other mammalian groups has yet to be unequivocally resolved, we suggest that a very early divergence of the group remains a distinct possibility.     

Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals

This study is based on the examination of histological sections of specimens of different ages and of adult ossicles from macerated skulls representing a wide range of taxa and aims at addressing several issues concerning the evolution of the ear ossicles in marsupials. Three-dimensional reconstructions of the ear ossicles based on histological series were done for one or more stages of Monodelphis domestica, Caluromys philander, Sminthopsis virginiae, Trichosurus vulpecula, and Macropus rufogriseus. Several common trends were found. Portions of the ossicles that are phylogenetically older develop earlier than portions representing more recent evolutionary inventions (manubrium of the malleus, crus longum of the incus). The onset of endochondral ossification in the taxa in which this was examined followed the sequence; first malleus, then incus, and finally stapes. In M. domestica and C. philander at birth the yet precartilaginous ossicles form a supportive strut between the lower jaw and the braincase. The cartilage of Paauw develops relatively late in comparison with the ear ossicles and in close association to the tendon of the stapedial muscle. A feeble artery traverses the stapedial foramen of the stapes in the youngest stages of M. domestica, C. philander, and Sminthopsis virginiae examined. Presence of a large stapedial foramen is reconstructed in the groundplan of the Didelphidae and of Marsupialia. The stapedial foramen is absent in all adult caenolestids, dasyurids, Myrmecobius, Notoryctes, peramelids, vombatids, and phascolarctids. Pouch young of Perameles sp. and Dasyurus viverrinus show a bicrurate stapes with a sizeable stapedial foramen. Some didelphids examined to date show a double insertion of the Tensor tympani muscle. Some differences exist between M. domestica and C. philander in adult ossicle form, including the relative length of the incudal crus breve and of the stapes. Several differences exist between the malleus of didelphids and that of some phalangeriforms, the latter showing a short neck, absence of the lamina, and a ventrally directed manubrium. Hearing starts in M. domestica at an age in which the external auditory meatus has not yet fully developed, the ossicles are not fully ossified, and the middle ear space is partially filled with loose mesenchyme. The ontogenetic changes in hearing abilities in M. domestica between postnatal days 30 and 40 may be at least partially related to changes in middle ear structures.     

Evolution and development of the mammalian jaw joint: Making a novel structure

A jaw joint between the squamosal and dentary is a defining feature of mammals and is referred to as the temporomandibular joint (TMJ) in humans. Driven by changes in dentition and jaw musculature, this new joint evolved early in the mammalian ancestral lineage and permitted the transference of the ancestral jaw joint into the middle ear. The fossil record demonstrates the steps in the cynodont lineage that led to the acquisition of the TMJ, including the expansion of the dentary bone, formation of the coronoid process, and initial contact between the dentary and squamosal. From a developmental perspective, the components of the TMJ form through tissue interactions of muscle and skeletal elements, as well as through interaction between the jaw and the cranial base, with the signals involved in these interactions being both biomechanical and biochemical. In this review, we discuss the development of the TMJ in an evolutionary context. We describe the evolution of the TMJ in the fossil record and the development of the TMJ in embryonic development. We address the formation of key elements of the TMJ and how knowledge from developmental biology can inform our understanding of TMJ evolution.     

A study of the os goniale in man.

The anterior process of the malleus of the middle ear develops irrespective of Meckel's cartilage through an intramembranous ossification center that appears in the human embryo of 26.5 mm crown-rump length at a caudomedial position in relation to Meckel's cartilage. The malleus has a double origin: the anterior process originates from the os goniale through intramembranous ossification, and the rest from Meckel's cartilage, through endochondral ossification.     

A phylogeny of the families of fossil and extant tetraodontiform fishes (Acanthomorpha, Tetraodontiformes), Upper Cretaceous to Recent

A data matrix is presented of 210 morphological characters (mostly osteological, some external) for 20 extant taxa of the ten Recent families of tetraodontiform fishes and 36 fossil tetraodontiforms. The oldest of these are from the Upper Cretaceous (95 Mya); most are from the Lower to Middle Eocene (50–58 Mya). There are two outgroup taxa (a zeiform and a caproid). A cladistic analysis of this matrix for only the extant taxa produced two equally parsimonious trees that call into question the monophyly of some of the previously accepted major higher-level tetraodontiform clades. Inclusion in the analysis of the large number of available fossil taxa helps to resolve relationships between family level clades. The new phylogenetic hypothesis, together with stratigraphic and biogeographical data, is used to discuss scenarios of the origin and evolution of the major clades of the order.  © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society , 2003, 139 , 565−617.     

Mammalian tooth marks on the bones of dinosaurs and other Late Cretaceous vertebrates

Abstract: We describe bones from the Late Cretaceous of Alberta – including bones of large dinosaurs, a femur from the aquatic reptile Champsosaurus, and a dentary from the marsupial Eodelphis– that bear tooth marks made by animals with opposing pairs of teeth. Of the animals known from the Late Cretaceous of North America, only mammals are capable of making such tooth marks. In particular, multituberculates, which have paired upper and lower incisors, are the most likely candidates for the makers of these traces. The traces described here represent the oldest known mammalian tooth marks. Although it is possible that some of these tooth marks represent feeding traces, the tooth marks often penetrate deep into the dense cortices of the bone. This raises the possibility that, much as extant mammals gnaw bone and antler, some Cretaceous mammals may have consumed the bones of dinosaurs and other vertebrates as a source of minerals. However, none of the tooth marks described here resemble the extensive gnaw traces produced by Cenozoic multituberculates or rodents. This suggests that specialized gnawing forms may have been rare or absent in the Late Cretaceous of North America.     

On the phylogenetic position of monotremes (Mammalia,Monotremata)

Henosferida from the Middle-Upper Jurassic of Western Gondwana is the most probable sister group for monotremes. They share the derived pretribosphenic structure of lower molars combined with the presumably absent protocone on the upper molars and the plesiomorphic retention of postdentary bones and pseudangular process of the lower jaw. In addition, the two groups share the dental formula with three molars and the position of the Meckel’s groove, which passes ventral to the mandibular foramen. In the course of subsequent evolution, monotremes acquired the mammalian middle ear with three auditory ossicles independently of therian mammals and multituberculates. Jurassic Laurasian Shuotheriidae are probably a sister group of the Gondwanian clade Henosferida + Monotremata. The Jurassic shuotheriid Pseudotribos shows a great plesiomorphic similarity to monotremes in the structure of the pectoral girdle, with a large interclavicle immovably connected to the clavicle. In the lineages leading to therian mammals and multituberculates, the pectoral girdle changed probably independently and in parallel in connection with the establishment of the parasagittal posture of the forelimbs (reduction of the interclavicle, mobile articulation of the interclavicle with clavicle, reduction of the procoracoid, and development of a supraspinous fossa of the scapula) and formation of the mammalian middle ear with three auditory ossicles.     

The Origin of the Mammalian Middle Ear

A functional explanation is presented for the shift of the reptilianarticular and quadrate into the mammalian middle ear to becomethe malleus and incus. Modification of the masticatory apparatusof therapsids results in reduction of stresses on the jaw jointand consequently in reduction of posterior elements of the jaw.In the late therapsid, Bienotherium, the quadrate and post-dentaryjaw bones resemble the mammalian malleus and incus which togetherform a lever. The therapsid articular possesses a downturnedretroarticular process (for insertion of M. depressor mandibulae)homologous with the manubrium (force lever arm) of the malleus.About the time of origin of the mammalian (dentarysquamosal)jaw joint and following the origin of the mammalian depressor,the reptilian depressor is lost. This allows the enlarging reptiliantympanum to become attached to the retroarticular process. Thenew lever system thus formed by articular and quadrate increasesthe sensitivity of the ear and the reptilian one-bone systemis replaced. In early mammals the reflected lamina of the angularmigrates posteriorly with the angle of the dentary so that itcontacts and assumes support of the tympanum. Non-homology ofthe monotreme and therian depressors indicates a multiple originof the mammalian middle ear.     

The female reproductive unit of Ephedra (Gnetales): comparative morphology and evolutionary perspectives

Morphological variation in Ephedra (Gnetales) is limited and confusing from an evolutionary perspective, with parallelisms and intraspecific variation. However, recent analyses of molecular data provide a phylogenetic framework for investigations of morphological traits, albeit with few informative characters in the investigated gene regions. We document morphological, anatomical and histological variation patterns in the female reproductive unit and test the hypothesis that some Early Cretaceous fossils, which share synapomorphies with Ephedra, are members of the extant clade. Results indicate that some morphological features are evolutionarily informative although intraspecific variation is evident. Histology and anatomy of cone bracts and seed envelopes show clade‐specific variation patterns. There is little evidence for an inclusion of the Cretaceous fossils in the extant clade. Rather, a hypothesized general pattern of reduction of the vasculature in the ephedran seed envelope, probably from four vascular bundles in the fossils, to ancestrally three in the living clade, and later to two, is consistent with phylogenetic and temporal analyses, which indicate that extant diversity evolved after the Cretaceous–Tertiary boundary. Notwithstanding striking similarities between living and Cretaceous Ephedra, available data indicate that the Mesozoic diversity went almost entirely extinct in the late Cretaceous causing a bottleneck effect in Ephedra, still reflected today by an extraordinarily low level of genetic and structural diversity. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163 , 387–430.     

Probable diphyletic formation of the mammalian middle ear: Monotremata and Theria

The first steps in the formation of the middle ear of the mammalian type, with the tympanum and three auditory ossicles, have only been passed by higher cynodonts. They have an incipient malleus, which developed from the anterior process of the articulare rather than the retroarticular process, which is rudimentary in cynodonts. The tympanic bone is formed of the anterior projections of the angulare. In some gorgonopians, the retroarticular process is elongated and curved anteriorly, resembling the malleus of mammals; however, this is only convergent similarity.