Comparative locomotor performance of marsupial and placental mammals

Marsupials are often considered inferior to placental mammals in a number of physiological characters. Because locomotor performance is presumed to be an important component of fitness, we compared marsupials and placentals with regard to both maximal running speeds and maximal aerobic speeds (=speed at which the maximal rate of oxygen consumption, VOlmax, is attained). Maximal aerobic speed is related to an animal's maximal sustainable speed, and hence is a useful comparative index of stamina.
Maximal running speeds of 11 species of Australian marsupials, eight species of Australian murid rodents, two species of American didelphid marsupials, and two species of American rodents were measured in the laboratory and compared with data compiled from the literature. Our values are greater than, or equivalent to, those reported previously. Marsupials and placentals do not differ in maximal running speeds (nor do Australian rodents differ from non-Australian rodents). Within these groups, however, species and families may differ considerably. Some of the interspecific variation in maximal running speeds is related to differences in habitat: species inhabiting open habitats (e.g. deserts) tend to be faster than are species from habitats with more cover, or arboreal species.
Maximal aerobic speeds (compiled from the literature) were higher in large species than in small species. However, marsupials and placentals show no general difference with regard to maximal aerobic speeds.
Maximal running speeds and maximal aerobic speeds for 18 species of mammals were not correlated, after correcting for correlations with body size. Thus, the fastest sprinters do not necessarily have high maximal aerobic speeds.     

Shape, variance and integration during craniogenesis: contrasting marsupial and placental mammals

Studies of morphological integration can provide insight into developmental patterns, even in extinct taxa known only from skeletal remains, thus making them an important tool for studies of evolutionary development. However, interpreting patterns of integration and assessing their significance for organismal evolution requires detailed understanding of the developmental interactions that shape integration and how those interactions change through ontogeny. Thus far, relatively little comparative data have been produced for this important topic, and the data that do exist are overwhelmingly from humans and their close relatives or from laboratory models such as mice. Here, we compare data on shape, variance and integration through postnatal ontogeny for a placental mammal, the least shrew, Cryptotis parva, and a marsupial mammal, the gray short-tailed opossum, Monodelphis domestica. Cranial variance decreased dramatically from early to late ontogeny in Cryptotis, but remained stable through ontogeny in Monodelphis, potentially reflecting functional constraints related to the short gestation and early ossification of oral bones in marsupials. Both Cryptotis and Monodelphis showed significant changes in cranial integration through ontogeny, with a mixture of increased, decreased and stable levels of integration in different cranial regions. Of particular note is that Monodelphis showed an unambiguous decrease in integration of the oral region through ontogeny, potentially relating to their early ossification. Selection at different stages of development may have markedly different effects if patterns of integration change substantially through ontogeny. Our results suggest that high integration of the oral region combined with functional constraints for suckling during early postnatal ontogeny may drive the stagnant variance observed in Monodelphis and potentially other marsupials.     

Functional capacities of marsupial hearts: size and mitochondrial parameters indicate higher aerobic capabilities than generally seen in placental mammals

This study of marsupial hearts explored the aerobic capacities of this group of mammals; recent information suggests that marsupials possess higher aerobic abilities than previously accepted. Characteristics such as heart mass, mitochondrial features and capillary parameters were examined. A comprehensive study of the heart of red kangaroos was included because of the high maximum oxygen consumption of this species. Goats were also included as a reference placental mammal. Marsupials have a heart that is generally larger than that of placentals. The allometric equation for the relationship between heart mass and body mass for marsupials was M_h=7.5M_b^0.944 (M_h in g and M_b in kg); the equivalent equation for placental mammals was M_h=6.0M_b^0.97. Mitochondrial volume density and inner mitochondrial surface density do not differ between the two mammal groups; although capillary parameters indicated a lower capillary volume in marsupials. Heart size appears to be the major difference between the two groups. The overall pattern seen in marsupials is similar to that of "athletic" placentals and indicates a relatively high aerobic potential.Abbreviations BMR basal metabolic rate - c(K,0) tortuosity factor - Jv(c,f) capillary length density - M_b body mass - M_h heart mass - N_A(c,f) numerical capillary density - r_c mean capillary radius - S(im,m) total surface area of inner mitochondrial membranes in the heart - Sv(im,m) surface density of the inner mitochondrial membranes - Sv(im,mt) surface density of inner mitochondrial membranes per unit volume of mitochondria - TEM transmission electron microscope - O₂max maximum aerobic capacity - V(mt,m) total mitochondrial volume - Vv(f,m) volume fraction of muscle occupied by muscle fibres - Vv(mt,f) mitochondrial volume densityCommunicated by I.D. Hume     

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.     

Western analyses of pregnancy-associated glycoprotein family (PAG) in placental extracts of various mammals

The present study was conducted in order to analyze the immunoreactivity of placental extracts of several animal species and humans against the following three groups of PAG antisera: anti-boPAG-I (R#497), -boPAG-II (R#435), and -caPAG (R#706). Placental proteins were obtained after extraction at neutral pH, followed by ammonium sulfate (A.S.) precipitation, dialysis, and lyophilization. The immunoreactivity of different placental extracts was revealed by the use of monodimensional SDS-PAGE, followed by blotting on nitrocellulose membrane and the identification of immunoreactive proteins after incubation with PAG antisera (Western blot technique). A strong immunoreactivity of proteins from synepitheliochorial placenta (cattle, sheep, goat, bison, buffalo, and deer) was demonstrated in both 20-50% and 50-80% A.S. fractions using the three antisera. Proteins from species with epitheliochorial placenta presented variable profiles of detected PAG-like proteins: in the sow, many immunoreactive forms were revealed by antisera boPAG-I and boPAG-II, whereas in the dromedary, only two forms were revealed by anti-boPAG-II. Concerning other species, our protocols showed for the first time a cross-reaction between PAG antisera with proteins extracted from dog, alpaca, dromedary, sea lion, and human placenta.     

Photopigment coexpression in mammals: comparative and developmental aspects

In mammals, each cone had been thought to contain only one single type of photopigment. It was not until the early 1990s that photopigment coexpression was reported. In the house mouse, the distribution of color cones shows a characteristic division. Whereas in the upper retinal field the ratio of short wave to middle-to-long wave cones falls in the usual range (1:10), in the ventral retinal field M/L-pigment expression is completely missing. In the transitional zone, numerous dual cones are detectable (spatial coexpression). In other species without retinal division, dual cones appear during development, suggesting that M/L-cones develop from S-cones. Dual elements represent a transitory stage in M/L-cone differentiation that disappear with maturation (transitory coexpression). These two phenomena seem to be mutually exclusive in the species studied so far. In the comparative part of this report the retinal cone distribution of eight rodent species is reported. In two species dual cones appear in adult specimens without retinal division, and dual elements either occupy the dorsal peripheral retina, or make up the entire cone population. This is the first observation proving that all cones of a retina are of dual nature. These species are good models for the study of molecular control of opsin expression and renders them suitable sources of dual cones for investigations on the role and neural connections of this peculiar cone type. In the developmental part, the retinal maturation of other species is examined to test the hypothesis of transitory coexpression. In these species S-pigment expression precedes that of the M/L-pigment, but dual cones are either identified in a small number or they are completely missing from the developing retina. These results exclude a common mechanism for M/L-cone maturation: they either transdifferentiate from S-cones or develop independently.     

The ear region of the marsupial sabertooth,Thylacosmilus: Influence of the sabertooth lifestyle upon it,and convergence with placental sabertooths

The mastoid auditory bulla of the extinct marsupial sabertooth, Thylacosmilus, has an enlarged, complex hypotympanic sinus but lacks an alisphenoid contribution. These are marked departures from the usual marsupial condition. Details of the ear region of Thylacosmilus are compared with those of the convergent, extinct placental sabertooth, Smilodon, and each is compared with less specialized related forms to define differences and similarities of the evolutionary paths that led to the striking overall convergence. Functional factors such as pressure transformer ratio (PTR), impedance transformer ratio (ITR), acoustic impedence at the eardrum, and the fraction of the sound energy theoretically transmitted to the inner ear cannot be estimated for Thylacosmilus because certain critical measures are still unknown (tympanum size, ossicle lever arm ratios). However, in both sabertooths enlarged complex hypotympanic sinuses, characterized by expansions and contractions, are greatly developed. They vastly increase middle ear space (volume) and must have influenced these factors. In both, the sinuses provide the large air volume needed to prevent excessive damping of sound energy transmission (Hunt and Korth, '80), and both are believed to have achieved a further modulation of the system from the cushioning or “pillow” effect of the confined air as it directly damps the tympanum itself. Thylacosmilus has still another feature that may have given greater control over damping of sound energy transmission: the direct opening (probably membrane covered) of one of the sinus cavities into the side of the meatal tube. In this feature, as in others noted earlier (Turnbull, '76, '78), we see a greater degree of specialization in this marsupial sabertooth than in a placental counterpart.     

Lung and metabolic development in mammals: contribution to the reconstruction of the marsupial and eutherian morphotype

Marsupials represent only 6% of all living mammals. Marsupialia and Placentalia are distinguished mainly by their modes of reproduction. In particular, the differences in the stage of development of the neonates may be one explanation for the divergent evolutionary success. In this respect one important question is whether the survivability of the neonate depends on the degree of maturation of the respiratory system relative to the metabolic capacity at the time of birth. Therefore, this review highlights the differences in lung morphology and metabolic development of extant Marsupialia and Placentalia. The Marsupial neonate is born with a low birth weight and is highly immature. The neonatal lung is characterized by large terminal sacs, a poorly developed bronchial system and late formation of alveoli. Marsupialia have a low metabolic rate at birth and attain adult metabolic rate and thermoregulatory capacity late in postnatal development. In contrast, the eutherian neonate is born with a relative high birth weight and is always more mature than marsupial neonates. The neonatal lung has small terminal sacs, the bronchial system is well developed and the formation of alveoli begins few days after birth. Placentalia have a high metabolic rate at birth and attain adult metabolic rate and thermoregulatory capacity early in postnatal development. The differences in the developmental degree of the newborn lung between Marsupialia and Placentalia have consequences for their metabolic and thermoregulatory capacity. These differences could be advantageous for Placentalia in the changing environments in which they evolved.     

Extensive intron gain in the ancestor of placental mammals

Background

Genetic plasticity may be understood as the ability of a functional gene network to tolerate alterations in its components or structure. Usually, the studies involving gene modifications in the course of the evolution are concerned to nucleotide sequence alterations in closely related species. However, the analysis of large scale data about the distribution of gene families in non-exclusively closely related species can provide insights on how plastic or how conserved a given gene family is. Here, we analyze the abundance and diversity of all Eukaryotic Clusters of Orthologous Groups (KOG) present in STRING database, resulting in a total of 4,850 KOGs. This dataset comprises 481,421 proteins distributed among 55 eukaryotes.

Results

We propose an index to evaluate the evolutionary plasticity and conservation of an orthologous group based on its abundance and diversity across eukaryotes. To further KOG plasticity analysis, we estimate the evolutionary distance average among all proteins which take part in the same orthologous group. As a result, we found a strong correlation between the evolutionary distance average and the proposed evolutionary plasticity index. Additionally, we found low evolutionary plasticity in Saccharomyces cerevisiae genes associated with inviability and Mus musculus genes associated with early lethality. At last, we plot the evolutionary plasticity value in different gene networks from yeast and humans. As a result, it was possible to discriminate among higher and lower plastic areas of the gene networks analyzed.

Conclusions

The distribution of gene families brings valuable information on evolutionary plasticity which might be related with genetic plasticity. Accordingly, it is possible to discriminate among conserved and plastic orthologous groups by evaluating their abundance and diversity across eukaryotes.

Reviewers

This article was reviewed by Prof Manyuan Long, Hiroyuki Toh, and Sebastien Halary.     

Heterochrony revisited: the evolution of developmental sequences

The concept of heterochrony is a persistent component of discussions about the way that evolution and development interact. Since the late 1970s heterochrony has been defined largely as developmental changes in the relationship of size and shape. This approach to heterochrony, here termed growth heterochrony, is limited in the way it can analyse change in the relative timing of developmental events in a number of respects. In particular, analytical techniques do not readily allow the study of changes in developmental events not characterized by size and shape parameters, or of many kinds of events in many taxa. I discuss here an alternative approach to heterochrony, termed sequence heterochrony, in which a developmental trajectory is conceptualized as a series of discrete events. Heterochrony is demonstrated when the sequence position of an event changes relative to other events in that sequence. I summarize several analytical techniques that allow the investigation of sequence heterochrony in phylogenetic contexts and also quantitatively. Finally, several examples of how this approach may be used to test hypotheses on the way development evolves are summarized.     

Mass-specific metabolic rate and sperm competition determine sperm size in marsupial mammals

Two complementary hypotheses have been proposed to explain variation in sperm size. The first proposes that post-copulatory sexual selection favors an increase in sperm size because it enhances sperm swimming speed, which is an important determinant of fertilization success in competitive contexts. The second hypothesis proposes that mass-specific metabolic rate acts as a constraint, because large animals with low mass-specific metabolic rates will not be able to process resources at the rates needed to produce large sperm. This constraint is expected to be particularly pronounced among mammals, given that this group contains some of the largest species on Earth. We tested these hypotheses among marsupials, a group in which mass-specific metabolic rates are roughly 30% lower than those of eutherian mammals of similar size, leading to the expectation that metabolic rate should be a major constraint. Our findings support both hypotheses because levels of sperm competition are associated with increases in sperm size, but low mass-specific metabolic rate constrains sperm size among large species. We also found that the relationship between sperm size and mass-specific metabolic rate is steeper among marsupials and shallower among eutherian mammals. This finding has two implications: marsupials respond to changes in mass-specific metabolic rate by modifying sperm length to a greater extent, suggesting that they are more constrained by metabolic rate. In addition, for any given mass-specific metabolic rate, marsupials produce longer sperm. We suggest that this is the consequence of marsupials diverting resources away from sperm numbers and into sperm size, due to their efficient sperm transport along the female tract and the existence of mechanisms to protect sperm.