Living and fossil placentals

The vast majority of living and fossil mammals are placentals. Today there are about 4,400 species, which are traditionally organised into 18 Orders, with an extra one if the Pinnipedia are separated from the Carnivora, and a twentieth if the recently extinct Malagasy order Bibymalagasia is recognised as such. There have been many attempts to discover supraordinal groupings from amongst these Orders based on morphological characters, though few proposals have been universally accepted. It is only with the advent of increasingly large sets of molecular sequence data in the last few years that a reasonably robust resolution looks imminent, although these contemporary analyses are remarkably and controversially at odds with the traditional ones. Novacek et al. (1988) summarised the then current situation regarding supraordinal classification of placentals, a time at which morphology was still dominant but molecular data was at the threshold of significance. They accepted a basal group Edentata that combined the Xenarthra of the New World with the Pholidota of the Old, based on a few cranial characters, loss of the anterior teeth, and reduction of the enamel of the remaining ones. This left the rest of the living placentals as a monophyletic group Epitheria, sharing such apparently minor characters as the shape of the stapes bone in the ear. They found very little resolution within the Epitheria, and concluded that there was a polychotomy of no less than nine lineages arranged as a ‘star’ phylogeny. No remnant of the previously recognised taxon Ferungulata, created by Simpson (1945) for the Carnivora plus the ungulate orders Artiodactyla, Perissodactyla, Proboscidea, Hyracoidea, Sirenia, and Tubulidentata remained. On the other hand, three supra ordinal taxa of earlier authors did survive. One was Gregory’s (1910) Archonta, consisting of generally conservative forms and by now composed of the Primates, Dermoptera, Scandentia, and Chiroptera, but excluding the Lipotyphla. The second was Glires, originating with Linnaeus (1758) and widely accepted ever since, for the Rodentia and Lagomorpha; Novacek et al. (1988) tentatively placed the Macroscelidea as the sister-group of the Glires. The third supraordinal taxon recognised was, like Glires, well-established if not universally accepted.

Living and fossil marsupials

There are about 265 living species of marsupial mammals, the majority in Australasia, about 60 in South America, and a handful in Central and North America (Macdonald 2001). They are distinguishable from the placental mammals by many characters, but most profoundly by their mode of reproduction. Compared to the placentals, there is only a relatively brief intrauterine period, during which the embryo exchanges nutrients and gases with the mother via a simple, non-invasive yolk sac placenta. There is no development of the complex, highly invasive chorio-allantoic placenta found in the placentals with the partial exception of the bandicoots in which there is a small, short-lived, but true chorio-allantoic placenta. The marsupial neonate is born at a very immature stage, and most of the total maternal provision comes via lactation. In the majority of cases the young are carried in a pouch, although there are exceptions to this. Whether pouched or not, the young attach themselves continuously to the teat for an extended period of time. There has been much discussion about whether the marsupial mode of reproduction is ancestral to that of the placental mammals, or whether it represents an independent, parallel acquisition of viviparity. Lillegraven (1979), Lillegraven et al. (1987), and Szalay (1994), for example, regarded the marsupial mode as primitive and inefficient compared to the placental mode, and that it was failure of the marsupials to evolve a mechanism to prevent immunological rejection of the embryo by the mother that prevented any extension of the gestation period. Placentals, they argued, solved the problem by evolving the trophoblast layer of embryonic cells that performs the function of preventing the maternal antibodies from damaging the embryo. Conversely, several authors such as Parker (1977) have argued that the marsupial mode is an alternative, but equally well-adapted strategy of reproduction to that of placentals. It is one of low investment but low risk, and is therefore suitable for a more unpredictable environment. Tyndale-Biscoe and Renfree (1987) suggested that primitive marsupials and placentals had quite similar reproduction, with relatively immature neonates and a relatively long lactation period. Subsequent specialisation in the two groups went in different directions.

Evolution of mammalian biology

There are large biological differences between the mammals and the primitive living amniotes as represented by turtles, lizards, and crocodiles ● Differentiated dentition with occluding post-canine teeth, and radical reorganisation of jaw musculature to operate them ● Differentiation of vertebral column and limb musculature, and repositioning of limbs to bring feet under the body, increasing agility of locomotion ● Relatively huge brain and highly sensitive sense organs ● Endothermic temperature physiology, with very high metabolic rates, insulation, and high respiratory rates ● Precise osmoregulatory and chemoregulatory abilities using loops of Henle in the kidney and an array of endocrine mechanisms Incomplete as it is, the fossil record of the mammal-like reptiles, or ‘non-mammalian synapsids’ permits the reconstruction of a series of hypothetical intermediate stages that offers considerable insight into how, when, and where this remarkable transition occurred. Deriving these stages starts with a cladogram of the relevant fossils that is then read as an evolutionary tree, with hypothetical ancestors represented by the nodes. The characters that define a node, plus the characters of the previous nodes, constitute the reconstruction. The differences in characters between adjacent nodes represent the evolutionary transitions that by inference occurred, and the whole set of successive nodes generates all that can be inferred about the sequence of acquisition of characters. If a hypothetical ancestral synapsid is placed at the base of the cladogram, and a hypothetical ancestral mammal as the final node, then the set of nodes in between represents everything the fossil record is capable of revealing about the pattern by which mammalian characters evolved: the sequence of their acquisition, the correlations between characters, and possibly the rates of their evolution. Of course, the inferred pattern of evolution of characters is only as reliable as the cladogram which generated it, and that in turn is only as realistic as the model of evolution used in its construction from the character data. And of course, there must have been many intermediate stages in the transition than cannot be reconstructed for want of appropriate fossil representation of those particular grades. Nevertheless, limited as it may be, this is what can be known from the fossil record.

The Mesozoic mammals

The expression ‘Mesozoic Mammals’ refers to more than simply the mammals of that particular period of time; it also stands for an extraordinary and quite mysterious concept. From the first appearance in rocks of Late Triassic times of the small, obviously highly active, large-brained animals thought of as mammals, through the following 145 million years of life on earth culminating in the great end-Cretaceous mass extinction that saw the end of the dinosaurs, these animals remained small. Although probably far from rare at the time, the great majority of species of Mesozoic mammals were of the size of shrews, rats, and mice. A tiny handful managed to evolve to the body size of foxes or beavers, but there were no representatives at all of mammals the size of the prominent mammals of today, the herbivorous horses, antelopes, and elephants, the lions and wolves that feed upon them, or the specialist apes, whales, and anteaters. Two points highlight just how odd this restriction in body size is. The first is that the Mesozoic mammals represent no less than two-thirds of mammalian evolution from their origin to the present, so there was plenty of time for evolution, and an extensive radiation did indeed occur producing a plethora of taxa. The second is that somewhere along the line, the potential for evolving large body size certainly existed because within, metaphorically speaking, moments of the end of the Mesozoic Era, middle-sized and soon thereafter large mammals had arisen and were flourishing. Since their very earliest recognition by Dean William Buckland (Buckland 1824) from the Middle Jurassic Stonesfield Slate of Oxfordshire, Mesozoic mammals have generated controversy (Desmond 1985). Transformationists like Robert Grant denied that they were mammals, because it disturbed their accepted temporal sequence of Mesozoic reptiles preceding the exclusively Tertiary mammals. On the other hand, establishment figures like Buckland himself and Sir Richard Owen welcomed this apparent refutation of transformationism and had no doubt that they were indeed opossum-like mammals. In the end, the true nature of these fossils was accepted, and by 1871, a good number of undoubtedly Mesozoic localities had yielded undoubtedly mammalian fossils.

Evolution of the mammal-like reptiles

Mammals, along with the biologically remarkably similar birds, are the vertebrates that are most completely adapted to the physiological rigours of the terrestrial environment. Whilst all the terrestrial dwelling tetrapods can operate in the absence of the buoyancy effect of water, and can use the gaseous oxygen available, mammals have in addition evolved a highly sophisticated ability to regulate precisely the internal temperature and chemical composition of their bodies in the face of the extremes of fluctuating temperature and the dehydrating conditions of dry land. From this perspective, the origin of mammalian biology may be said to have commenced with the emergence of primitive tetrapods onto land around 370 Ma, in the Upper Devonian. Until the 1990s, the only Devonian tetrapod at all well known was Ichthyostega from east Greenland, as described by Jarvik (e.g. Jarvik 1980, 1996). Famous for its combination of primitive fishlike characters such as the lateral line canals, bony rays supporting a tail fin, and remnants of the opercular bones, with fully tetrapod characters such as the loss of the gills and opercular cover, robust ribcage, and of course large feet with digits, Ichthyostega provided more or less all the fossil information there was relating to the transition from a hypothetical rhipidistian fish to a tetrapod. Subsequently, however, an ever-increasing number of other Upper Devonian tetrapods have been described, and the emerging picture of the origin of vertebrate terrestriality has become more complicated and surprising (Ahlberg and Milner 1994; Clack 2002). The earliest forms are Upper Frasnian in age, and include Elginerpeton from the Scottish locality of Scat Craig (Ahlberg 1995, 1998). So far known only from a few bones of the limbs and jaws, Elginerpeton adds little detail to the understanding of the evolution of tetrapods except to demonstrate that the process had commenced at least 10 million years prior to the existence of Ichthyostega. The next oldest tetrapods are Fammenian in age and include Ichthyostega, and a second east Greenland form, Acanthostega, which has been described in great detail (Coates and Clack 1990, 1991; Coates 1996).

Time and classification

The age and the classification of a particular fossil are the two fundamental properties necessary to begun understanding how it fits into the evolutionary patterns revealed by the fossil record. There are often misunderstandings of one or other of these by specialists. Evolutionary biologists on occasion express far too optimistic a view of how accurately fossils can actually be dated, both absolutely and relative to one another. Geologists have been known to have a rather limited view of how modern systematic methods are used to infer relationships from large amounts of information, be it morphological or molecular. In this chapter, a brief outline of the principles underlying the construction of the geological timescale, and of a classification are given, along with reference timescales and classifications for use throughout the following chapters. The creation of a timescale for dating the events recorded in the rocks since the origin of the Earth is one of the greatest achievements of science, unspectacular and taken for granted as it may often be. It is also unfinished business insofar as there are varying degrees of uncertainty and inaccuracy about the dates of many rock exposures, none more so than among the mostly continental, rather than marine sediments containing the fossils with which this work is concerned. A geological timescale is actually a compilation of the results of two kinds of study. One is recognising the temporal sequence of the rocks, and agreeing arbitrarily defined boundaries between the named rock units, the result of which is a chronostratic timescale. The other is calibration of the sequence and its divisions in absolute time units of years before present, a chronometric timescale. It is simple in principle to list the relative temporal order of events, such as the occurrence of fossils, in a single rock unit, although even here the possibility of missing segments, known as hiatuses, in local parts of the unit, or of complex folding movements of the strata disturbing the order must not be forgotten. The biggest problem is correlating relative dates between different units in different parts of the world.

Introduction

There are about 4,600 species of animals today that are called mammals because, despite an astonishing diversity of form and habitat, they all share a long list of characters not found in any other organisms, such as the presence of mammary glands, the single bone in the lower jaw, and the neocortex of the forebrain. This makes them unambiguously distinct from their closest living relatives, and their unique characters together define a monophyletic taxon, the class Mammalia. Three subgroups are readily distinguished amongst the living mammals. The Monotremata are the egg-laying mammals of Australasia, consisting only of two species of echidna and a single platypus species; for all their primitive reproductive biology, monotremes are fully mammalian in their general structure and biology. The Marsupialia, or Metatheria are the pouched mammals, whose approximately 260 species dominate the mammalian fauna of Australia, and also occur as part of the indigenous fauna of the Americas. By far the largest group of living mammals are the Placentalia, or Eutheria with about 4,350 species divided into usually eighteen recent orders. It is virtually unanimously accepted that the closest living relatives, the sister group, of mammals consists of the reptiles and the birds. The only serious dissent from this view in recent years was that of Gardiner (1982) who advocated that the birds alone and mammals were sister groups, the two constituting a taxon Haemothermia, defined among other characters by the endothermic (‘warm-blooded’) temperature physiology. Gardiner certainly drew attention to some remarkable similarities between birds and mammals, notably the details of the endothermic processes, the enlarged size and surface folding of the cerebellum, and a number of more superficial morphological features. There was also some molecular sequence data supporting the Haemothermia concept, including the beta-globin gene and 18S rRNA. Gardiner’s view briefly became a cause célèbre in part for its sheer heterodoxy, but all concerned have since rejected it on the grounds that a careful, comprehensive analysis of the characters supports the traditional view (Kemp 1988b), particularly if the characters of the relevant fossils are taken into account (Gauthier, Kluge, and Rowe 1988).