The evolutionary and morphological history of the parasphenoid bone in vertebrates

The parasphenoid is located in the cranium of many vertebrates. When present, it is always an unpaired, dermal bone. While most basal vertebrates have a parasphenoid, most placental mammals lack this element and have an unpaired, dermal vomer in a similar position (i.e. associated with the same bones) and with a similar function. As such, the parasphenoid and the vomer were considered homologous by some early twentieth century researchers. However, others questioned this homology based on comparisons between mammals and reptiles. Here we investigate the parasphenoid bone across the major vertebrate lineages (amphibians, reptiles, mammals and teleosts) including both developmental and evolutionary aspects, which until now have not been considered together. We find that within all the major vertebrate lineages there are organisms that possess a parasphenoid and a vomer, while the parasphenoid is absent within caecilians and most placental mammals. Based on our assessment and Patterson's conjunction tests, we conclude that the non‐mammalian parasphenoid and the vomer in mammals cannot be considered homologous. Additionally, the parasphenoid is likely homologous between sarcopterygian and actinopterygian lineages. This research attempts to resolve the issue of the parasphenoid homology and highlights where gaps in our knowledge are still present.     

The relationship between body mass and relative investment in testes mass in cetaceans: Implications for inferring interspecific variations in the extent of sperm competition

Based on sperm competition theory, percentage testes mass (% of total body mass) has been used to infer variations in the extent of sperm competition within mating systems of cetaceans. However, in most amniote taxa, including mammals, there is an underlying negative relationship between body mass and relative investment in testes mass, which must first be taken into account. Here, I identify a very strong nonlinear, negative relationship between body mass in cetaceans and relative investment in testes mass based on data from 31 species. As a result, if percentage testes mass alone is used to infer the relative extent of sperm competition in cetaceans, its importance in mating systems of smaller species is likely to be overestimated, whereas its role in larger species is likely to be underestimated. Similarly, there will also be systematic biases if this relationship is assumed to be linear when it is not. Therefore, it is essential that the underlying, nonlinear body mass–testes mass relationship is correctly taken into account when using relative investment in testes mass to estimate the relative levels of sperm competition in cetaceans. This is particularly important if such inferences are used to inform conservation strategies for endangered cetacean species.     

A Phylogenetic Perspective on Locomotory Strategies in Early Amniotes

Past approaches to understanding the evolution of locomotorystrategies among Paleozoic amniotes ("primitive reptiles" ofprevious parlance) have been influenced by preservational bias:early occurrences of some amniote taxa were used to polarizethe acquisition or development of locomotory structures amongthe earliest amniotes. Using a phylogeny representing the currentconsensus in the literature, we investigate the major locomotorystrategies that have been posited for Paleozoic amniotes (basalsynapsids on one hand and early reptiles on the other) by optimizingthe major locomotory styles identified for these taxa onto theconsensus tree, in order to present an overview of the patternof evolution of locomotory strategies inherited and adoptedby various amniote lineages.     

Evolution of amniote dentine apposition rates

In amniotes, daily rates of dentine formation in non-ever-growing teeth range from less than 1 to over 25 μm per day. The latter value has been suggested to represent the upper limit of odontoblast activity in non-ever-growing teeth, a hypothesis supported by the lack of scaling between dentine apposition rates and body mass in Dinosauria. To determine the correlates and potential controls of dentine apposition rate, we assembled a dataset of apposition rates, metabolic rates and body masses for ca 80 amniote taxa of diverse ecologies and diets. We used phylogenetic regression to test for scaling relationships and reconstruct ancestral states of daily dentine apposition across Amniota. We find no relationship between body mass and daily dentine apposition rate (DDAR) for non-ever-growing teeth in Amniota as a whole or within major clades. Metabolic rate, the number of tooth generations, diet and habitat also do not predict or correspond with DDARs. Similar DDARs are found in large terrestrial mammals, dinosaurs and marine reptiles, whereas primates, cetaceans and some smaller marine reptiles independently evolved exceptionally slow rates. Life-history factors may explain the evolution of dentine apposition rates, which evolved rapidly at the origin of major clades.     

BioEssays 10/2020

Frequent independent origins of environmental sex determination (ESD) are assumed within amniotes. However, the phylogenetic distribution of sex-determining modes suggests that ESD is likely very ancient and may be homologous across ESD groups. Sex chromosomes are demonstrated to be old and stable in endothermic (mammals and birds) and many ectothermic (non-avian reptiles) lineages, but they are mostly non-homologous between individual amniote lineages. The phylogenetic pattern may be explained by ancestral ESD with multiple transitions to later evolutionary stable genotypic sex determination. It is pointed out here that amniote ESD shares several key aspects with sequential hermaphroditism of fishes such as a lack of sex differences in genomes, biased population sex ratios, and potentially also molecular mechanism related to general stress responses. Here, it is speculated that ESD evolves via a heterochronic shift of the sensitive period of sex change from the adult to the embryonic stage in a hermaphroditic amniote ancestor. Also see the video abstract here https://youtu.be/q2mjtlCefu4 .     

Germline development in amniotes: A paradigm shift in primordial germ cell specification

In the field of germline development in amniote vertebrates, primordial germ cell (PGC) specification in birds and reptiles remains controversial. Avians are believed to adopt a predetermination or maternal specification mode of PGC formation, contrary to an inductive mode employed by mammals and, supposedly, reptiles. Here, we revisit and review some key aspects of PGC development that channelled the current subdivision, and challenge the position of birds and reptiles as well as the ‘binary’ evolutionary model of PGC development in vertebrates. We propose an alternative view on PGC specification where germ plasm plays a role in laying the foundation for the formation of PGC precursors (pPGC), but not necessarily of PGCs. Moreover, inductive mechanisms may be necessary for the transition from pPGCs to PGCs. Within this framework, the implementation of data from birds and reptiles could provide new insights on the evolution of PGC specification in amniotes.     

Relationships between species richness of vascular plants and terrestrial vertebrates in China: analyses based on data of nature reserves

The relationship between plant diversity and animal diversity on a broadscale and its mechanisms are uncertain. In this study, we explored this relationship and its possible mechanisms using data from 186 nature reserves across China on species richness of vascular plants and terrestrial vertebrates, and climatic and topographical variables. We found significant positive correlations between species richness in almost all taxa of vascular plants and terrestrial vertebrates. Multiple regression analyses indicated that plant richness was a significant predictor of richness patterns for terrestrial vertebrates (except birds), suggesting that a causal association may exist between plant diversity and vertebrate diversity in China. The mechanisms for the relationships between species richness of plants and animals are probably dependent on vertebrate groups. For mammals (endothermic vertebrates), this relationship probably represents the integrated effects of plants on animals through trophic links (i.e. providing foods) and non-trophic interactions (i.e. supplying habitats), whereas for amphibians and reptiles (ectothermic vertebrates), this may be a result of the non-trophic links, such as the effects of plants on the resources that amphibians and reptiles require.     

Embryonic keratinization in vertebrates in relation to land colonization

The embryogenesis and cytology of the epidermis in different vertebrates is variable in relation to the formation of a stratum corneum of different complexity. The latter process was essential for land colonization during vertebrate evolution and produced an efficient barrier in amniotes. Keratinocytes are made of cross‐linked keratins associated with specific proteins and lipids that are produced at advanced stages of embryogenesis when the epidermis becomes stratified. In these stages the epidermis changes from an aquatic to a terrestrial type, preadapted in preparation for the impact with the dry terrestrial environment that occurs at hatching or parturition. The epidermal barrier against water‐loss, mechanical and chemical stress, and microbe penetration is completely formed shortly before birth. Beneath the outer periderm, variably stratified embryonic layers containing glycine‐rich alpha‐keratins are formed in preparation for adult life. The following layers of the epidermis produce proteins for the formation of the cornified cell membrane and of the cornified material present in keratinocytes of the adult epidermis in reptiles, birds and mammals. The general features of the process of soft cornification in the embryonic epidermis of vertebrates are presented. Cornification in developing scales in reptiles, avian feathers and mammalian hairs is mainly related to the evolution of keratin‐associated proteins. The latter proteins form the resistant matrix of hard skin derivatives such as claws, beaks, nails and horns.     

The Oldest Caseid Synapsid from the Late Pennsylvanian of Kansas,and the Evolution of Herbivory in Terrestrial Vertebrates

The origin and early evolution of amniotes (fully terrestrial vertebrates) led to major changes in the structure and hierarchy of terrestrial ecosystems. The first appearance of herbivores played a pivotal role in this transformation. After an early bifurcation into Reptilia and Synapsida (including mammals) 315 Ma, synapsids dominated Paleozoic terrestrial vertebrate communities, with the herbivorous caseids representing the largest vertebrates on land. Eocasea martini gen. et sp. nov., a small carnivorous caseid from the Late Carboniferous, extends significantly the fossil record of Caseidae, and permits the first clade-based study of the origin and initial evolution of herbivory in terrestrial tetrapods. Our results demonstrate for the first time that large caseid herbivores evolved from small, non-herbivorous caseids. This pattern is mirrored by three other clades, documenting multiple, independent, but temporally staggered origins of herbivory and increase in body size among early terrestrial tetrapods, leading to patterns consistent with modern terrestrial ecosystem.     

Long-bone circumference and weight in mammals, birds and dinosaurs

The mid-shaft circumferences of the humerus and femur are closely related to body weight in living terrestrial vertebrates. Because these elements are frequently preserved in subfossil and fossil vertebrate skeletal materials, the relationship can be used to estimate body weight in extinct vertebrates. When the allometric equations are applied to the mid-shaft circumferences of these elements in dinosaurs, the weights calculated for some giant sauropods ( Brachiosaurus ) are found to be lighter than previous estimates.     

Has the importance of the amniote egg been overstated?

The evolution of the amniote egg is commonly regarded as an important milestone in the history of the vertebrates, an innovation that completed the transition from aquatic to fully terrestrial existence by permitting eggs to be laid away from standing water. This view derives ultimately from the recapitulationist theories of Haeckel, and rests on the assumption that extant frogs and salamanders are good models for the reproductive habits of early tetrapods and the ancestors of the amniotes. It also assumes that it is more difficult to lay eggs on land than in water, and that the amniote egg is an adaptation to the physical rigours that eggs encounter in terrestrial environments. Taken together, these assumptions comprise what may be termed the 'Haeckelian framework' for the origin of vertebrate terrestriality. Several independent lines of evidence suggest that the assumptions of the Haeckelian framework are false. There appear to be no theoretical reasons to assume that the evolution of terrestrial egg-laying was difficult, or required a structure as elaborate as the amniote egg. The physical conditions eggs encounter in the terrestrial environments where they are actually laid are quite mild. Land may in fact be an easier place to lay eggs than water. In addition, analysis of the distribution of key reproductive character states among vertebrates provides no evidence that the 'typical amphibian' reproductive mode is primitive for tetrapods. Amniotes are as likely as frogs or salamanders to retain primitive reproductive character states.     

Ovarian steroid synthesis and the hormonal control of the elasmobranch reproductive tract

Synopsis The reproductive biology of the chondricthyan fishes is remarkably sophisticated. Using both oviparous and viviparous reproductive modes, the group has generally adapted the style of bringing forth relatively few young at one time, each representing the investment of a great deal of maternal energy. The oviparous species foreshadow the situation common in oviparous reptiles and universal in birds. On the other hand, viviparous species range from simple internal incubators, in which large yolked eggs are retained, to other species in which the complexity of placentation and yolk reduction approach the eutherian condition. Further, in certain viviparous elasmobranchs the phenomenon of histotrophic nutrition attains an importance and complexity not seen in any other vertebrate group including mammals. Internal fertilization and amniote patterns of reproductive tract development also operate in virtually all elasmobranchs. The summary of work presented here suggests that these female reproductive styles are associated with a reproductive endocrinology which is the archetype for amniote vertebrates.     

The evolution of the mechanical properties of amniote bone

162 specimens from 19 species of amniote were tested for various mechanical and physical properties to ascertain whether there were characteristic differences between different groups. All mechanical properties showed very great variation. In general the reptiles were not inferior to the mammals and birds. The histology of living forms was compared to that of fossil forms, to see whether 'weak' histology was more characteristic of primitive amniotes. The earliest reptiles probably had rather complaint bone, but it was probably tough. Modern types of bone appeared over two hundred million years ago. Very specialised bone, like that of the bullae of whales and antlers, may have evolved only in the mammals, but the fossil record is not complete enough to assert this confidently.     

Arthropod remains in the oral cavities of fossil reptiles support inference of early insectivory

Inference of feeding preferences in fossil terrestrial vertebrates (tetrapods) has been drawn predominantly from craniodental morphology, and less so from fossil specimens preserving conclusive evidence of diet in the form of oral and/or gut contents. Recently, the pivotal role of insectivory in tetrapod evolution was emphasized by the identification of putative insectivores as the closest relatives of the oldest known herbivorous amniotes. We provide the first compelling evidence for insectivory among early tetrapods on the basis of two 280-million-year-old (late Palaeozoic) fossil specimens of a new species of acleistorhinid parareptile with preserved arthropod cuticle on their toothed palates. Their dental morphology, consisting of homodont marginal dentition with cutting edges and slightly recurved tips, is consistent with an insectivorous diet. The intimate association of arthropod cuticle with the oral region of two small reptiles, from a rich fossil locality that has otherwise not produced invertebrate remains, strongly supports the inference of insectivory in the reptiles. These fossils lend additional support to the hypothesis that the origins and earliest stages of higher vertebrate evolution are associated with relatively small terrestrial insectivores.     

Allometry of Reproduction in Poikilotherm and Homoiotherm Vertebrates

A comparison of 26 allometric empiric equations relating animal body weight and progeny weight, size and weight of the clutch, as well as the accompanying processes in various classes of vertebrates has revealed a principle of large-scale transformation specific for poikilotherms and two others specific for homoiotherm birds and mammals. The appearance of huge terrestrial eggs in reptiles and the transition from R-strategy to k-strategy was not accompanied by a rearrangement of the poikilotherm principle of reproduction pattern. Such rearrangement was required after the appearance of homoiotherm embryo and obligate parental care.     

Allometric scaling of seed retention time in seed dispersers and its application to estimation of seed dispersal potentials of theropod dinosaurs

Seed retention time (SRT), the time interval between seed ingestion and defaecation, is a critical parameter that determines the spatial pattern of seed dispersal created by an animal, and is therefore, an essential component of trait‐based modelling of seed dispersal functions. However, no simple predictive model of SRT for any given animal exists. We explored the linkage between animal traits and SRT. We collected previously published data on mean SRT for 112 species of birds, mammals, reptiles and fishes and investigated the general allometric scaling of mean SRT with body mass for each taxon. Moreover, we analysed the effects of food habit and digestive strategy on mean SRT for birds and mammals. In general, mean SRT increased with body mass in all four taxa, whereas the pattern of allometric scaling varied greatly among the taxa. Birds had a smaller intercept and larger slope than those of mammals, whereas reptiles had a much larger intercept and smaller slope than those of either birds or mammals. For birds, food habit was also detected as an important factor affecting SRT. We applied the allometric scaling that was obtained for birds to estimate mean SRT of extinct Mesozoic dinosaurs (Theropoda) – few of which are assumed to have acted as seed dispersers. SRT for large carnivorous theropods was estimated to be 4–5 days, when considering only body mass. The present study provides allometric scaling parameters of mean SRT for a variety of seed‐dispersing animals, and highlights large variations in scaling among taxa. The allometric scaling obtained could be a critical component of further trait‐based modelling of seed dispersal functions. Further, the potential and limitations of the scaling of animal SRT with body mass and a future pathway to the development of trait‐based modelling are discussed.     

Changes in body temperature pattern in vertebrates do not influence the codon usages of alpha-globin genes

Codon usages are known to vary among vertebrates chiefly due to variations in isochore structure. Under the assumption that marked differences exist in isochore structure between warm-blooded and cold-blooded animals, the variations among vertebrates were previously attributed to an adaptation to homeothermy. However, based on data from a turtle species and a crocodile (Archosauromorpha), it was recently proposed that the common ancestors of mammals, birds and extent reptiles already had the "warm-blooded" isochore structure. We determined the nucleotide sequences of alpha-globin genes from two species of heterotherms, cuckoo (Cuculus canorus) and bat (Pipistrellus abramus), and three species of snakes (Lepidosauromorpha), Naja kaouthia from a tropical terrestrial habitat, Elaphe climacophora from a temperate terrestrial habitat, and Hydrophis melanocephalus from a tropical marine habitat. Our purposes were to assess the influence of differential body temperature patterns on codon usage and GC content at the third position of a codon (GC3), and to test the hypothesis concerning the phylogenetic position at which GC contents had increased in vertebrates. The results of principal component analysis (PCA) using the present data and data for other taxa from GenBank indicate that the primary difference in codon usage in globin genes among amniotes and other vertebrates lies in GC3. The codon usages (and GC3) in alpha-globin genes from two heterotherms and three snakes are similar to those in alpha-globin genes from warm-blooded vertebrates. These results refute the influence of body temperature pattern upon codon usages (and GC3) in alpha-globin genes, and support the hypothesis that the increase in GC content in the genome occurred in the common ancestor of amniotes.     

Recruitment of 5' Hoxa genes in the allantois is essential for proper extra-embryonic function in placental mammals

The Hox gene family is well known for its functions in establishing morphological diversity along the anterior-posterior axis of developing embryos. In mammals, one of these genes, Hoxa13, is crucial for embryonic survival, as its function is required for the proper expansion of the fetal vasculature in the placenta. Thus, it appears that the developmental strategy specific to placental mammals is linked, at least in part, to the recruitment of Hoxa13 function in developing extra-embryonic tissues. Yet, the mechanism underlying this extra-embryonic recruitment is unknown. Here, we provide evidence that this functional novelty is not exclusive to Hoxa13 but is shared with its neighboring Hoxa11 and Hoxa10 genes. We show that the extra-embryonic function of these three Hoxa genes stems from their specific expression in the allantois, an extra-embryonic hallmark of amniote vertebrates. Interestingly, Hoxa10-13 expression in the allantois is conserved in chick embryos, which are non-placental amniotes, suggesting that the extra-embryonic recruitment of Hoxa10, Hoxa11 and Hoxa13 most likely arose in amniotes, i.e. prior to the emergence of placental mammals. Finally, using a series of targeted recombination and transgenic assays, we provide evidence that the regulatory mechanism underlying Hoxa expression in the allantois is extremely complex and relies on several cis-regulatory sequences.