MARSUPIAL AND MONOTREME EVOLUTION

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1 In: Marsupials and Monotremes ISBN: Editors: A. Klieve, L. Hogan, S. Johnston, P. Murray 2015 Nova Science Publishers, Inc. Chapter 1 MARSUPIAL AND MONOTREME EVOLUTION AND BIOGEOGRAPHY Vera Weisbecker 1, * and Robin M. D. Beck 2 1 School of Biological Sciences, University of Queensland, St Lucia, Queensland, Australia 2 School of Environment and Life Sciences, University of Salford, Manchester, England ABSTRACT This chapter provides an evolutionary context to comparative research on monotremes and marsupials. It explains the evolutionary origins of the three major living mammalian clades from within the ancient amniote lineage of synapsids, summarises their most obvious biological differences, and briefly outlines the difference between the terms Monotremata, Marsupialia and Placentalia vs. Prototheria, Metatheria and Eutheria. The living monotreme and marsupial families are introduced via short characterisations of their general biology and evolution. An up-to-date family-level phylogeny is provided for marsupials, together with a summary of our past and current understanding of their phylogenetic relationships. The known fossil record and biogeography of both radiations is summarised; particular attention is given to a recent paradigm shift on monotreme evolution, with the latest research suggesting that monotremes are part of an ancient, Gondwanan radiation of mammals that independently evolved a tribosphenic dentition. The unusual biogeographical history of marsupials and their extinct relatives, including a probable origin in the northern continents and later distribution across South America, Antarctica, and Australia, is also discussed. Keywords: mammalia, prototheria, metatheria, marsupialia, synapsida, phylogenetics, biogeography, gondwana, marsupionta, syndactyla, polyprotodonta * Corresponding author: Vera Weisbecker. v.weisbecker@uq.edu.au.

2 2 Vera Weisbecker and Robin M. D. Beck INTRODUCTION The study of marsupial and monotreme evolution and biogeography has a long and illustrious history. Many of the most prominent scientists of the last two centuries have contributed to this field, resulting in anecdotes, controversies, and unexpected twists, some of which are covered in this chapter. Many of the debates of old are now settled, while others are still continuing with a vigour that reveals this superficially dusty-looking topic to be an exciting and vibrant research field. A deep-time evolutionary perspective helps to understand the long-standing scientific interest in marsupials and monotremes. At least 310 million years ago, the lineage leading to mammals called the synapsids diverged from other vertebrates (Kemp 2005). The earliest synapsids were quite small, but many representatives of the lineage were large animals, such as the famous, superficially dinosaur-like Dimetrodon with its dorsal sail (Kemp 2005). Today, all that is left of the synapsids are the mammals (class Mammalia), which includes today s living marsupials, monotremes, and placentals (Figure 1). By any standard, mammals are not your usual vertebrate (Kemp 2005); they are furry and endothermic (able to metabolically elevate their body temperature over ambient temperatures), and ancestrally they were characterised by small body size compared to most other synapsids. Their reproduction is drastically different from other living amniotes, such as lizards and birds, because of their unique combination of intra-uterine pregnancy, lactation, and extended maternal care. They also have reduced the number of bones in their skull and skeleton (Kemp 2005). Their brains have ballooned, and with them their intelligence (Rowe et al. 2011). Parts of the original jaw joint have moved into the middle ear to form the mammalian ear ossicles (Luo 2007). The dentition of most mammals is highly specialised and particularly efficient at processing food (Kemp 2005). At some point, one lineage of synapsids acquired the ability to diversify morphologically and physiologically to a degree that no single terrestrial vertebrate group had previously managed, and today mammals include some extremely derived forms, such as the fully aquatic whales, hopping kangaroos, electrosensitive platypus, and several types of moles whose skeletal shape almost defies belief. The fossil record provides a limited amount of clues on how mammalness originated (Luo 2007). However, the many mammalian soft-tissue and physiological traits for example lactation, endothermy, and development rarely leave direct fossil evidence. Their evolution can only be inferred through comparison between the three remaining major mammalian groups that are left and determining what the common denominator of the three is (Weisbecker 2011). Luckily, each of the mammalian clades is quite distinctive and useful in understanding not only what the ancestral mammalian conditions were, but also what variations on this theme are possible within mammals. Table 1 lists some of the most obvious differences between the presumed ancestral conditions of the three clades. Montremes and marsupials retain some traits that are probably ancestral for mammals as a whole, which, if properly established (see Chapter 11) makes them useful for understanding ancestral mammalian biology. In addition, marsupials in particular offer a substantial advantage to the biomedical and veterinary sciences because the vast majority of their development occurs outside the womb, which means that most developmental processes can be observed without the need for surgical intervention on females (Selwood & Coulson 2006).

3 Marsupial and Monotreme Evolution and Biogeography 3 Table 1. Some of the differences between the ancestral body plans of monotremes, marsupials, and placentals Monotremes Marsupials Placentals Oviparous (egg-laying) Viviparous (live birth) Viviparous (live birth) Altricial (immature) Altricial neonates crawl to mother s Precocial (mature-born) neonates hatchlings nipple Milk field lactation Nipple lactation with phase of Nipple lactation, no attachment (nipples absent) nipple attachment Short gestation Short gestation (as little as 12 days in some bandicoots) Long gestation (as long as 22 months in the case of African Elephants) Long lactation, Long lactation, in pouch Variable lactation pouch/nest Retain a separate No separate coracoid No separate coracoid coracoid bone in the shoulder girdle Electrosensitive bill/beak No electrosensitivity No electrosensitivity Very low living diversity (1 platypus species and 4 echidna species) Higher living diversity, >330 described species Highest living diversity, >4500 described species Marsupials/Monotremes or Metatherians/Prototherians? Before discussing the evolution of marsupials and monotremes, we need to clarify the difference between two different sets of taxonomic terms that are at times used interchangeably for the three main modern mammalian radiations: Monotremata, Marsupialia and Placentalia vs. Prototheria, Metatheria, and Eutheria (see also Figure 1). The probably more familiar Monotremata, Marsupialia and Placentalia are the so-called crown groups (Williamson et al. 2014). Crown groups are defined as comprising the extant (living) species, their common ancestor, and all extinct species that share this common ancestor (Jefferies 1979). The crown group is augmented by the broader definitions of Prototheria, Metatheria and Eutheria (Williamson et al. 2014). These total-groups each comprise a particular crown group and any extinct species that are more closely related to that crown group than they are to any other living clade (Jefferies 1979). Extinct species that are members of the total group but not the crown group are referred to as stem-taxa. For example: the extinct mammal Sinodelphys is more closely related to marsupials than to monotremes or placentals, but it is not related to any specific living marsupial; its position on the marsupial stem makes it member of Metatheria (= the total group) but not Marsupialia (= the crown group) (Figure 1). By contrast, the recently extinct thylacine (or Tasmanian tiger ) is a close relative of living dasyuromorphians (dasyurids and the numbat) and therefore is not only a metatherian but also a marsupial. As discussed in the last chapter, the terms of Prototheria, Metatheria and Eutheria are the historical relic of an inappropriate teleological ( goal-oriented ) terminology that placed humans as the pinnacle of mammalian evolution (Huxley 1880).

4 4 Vera Weisbecker and Robin M. D. Beck Box 1. How do monotremes, marsupials, and placentals fit together? The short answer is: marsupials and placentals form a monophyletic group, called Theria, to the exclusion of monotremes (Figure 1). However, this answer hides an intriguing debate on the phylogenetic relationships of the three living mammalian clades. It is worth mentioning as it shows how important an accurate phylogeny is to the understanding of how mammalian body plans evolve. Until recently, the hypothesis that marsupials and monotremes form a clade to the exclusion of placentals had been considered possible; this hypothesised clade was named Marsupionta. Since originally being proposed nearly 70 years ago (Gregory 1947), there was never much support for the Marsupionta hypothesis (Kirsch & Mayer 1998) and it had been almost forgotten until several publications from the rapidly expanding field of molecular phylogenetics found seemingly strong support for Marsupionta as a clade (Janke et al. 2002), causing much excitement in the scientific community. The implications would have been farreaching: monophyly of Marsupionta would mean that many key traits shared by marsupials and placentals evolved independently (a pattern called convergence ); these include live birth, nipples, loss of the coracoid bone, and probably a raised metabolic rate, among many other traits. However, subsequent molecular studies, including work by the same authors who had previously retrieved Marsupionta (e.g., Kullberg et al. 2008), showed beyond reasonable doubt that marsupials and placentals are sister groups after all. Figure 1. Overview of the phylogenetic relationships and divergence times between monotremes, marsupials, and placentals, including the earliest known stem representatives of each clade. Divergence estimates and fossil ages are based on (Luo et al. 2003; Phillips et al. 2009; Luo et al. 2011).

5 Marsupial and Monotreme Evolution and Biogeography 5 Unfortunately, the crown-group names Monotremata, Marsupialia, and Placentalia are also perhaps not ideal (Tyndale-Biscoe 2005): Monotremata means one hole, referring to the monotreme cloaca (a single exit for the intestinal, reproductive, and urinary tracts), but marsupials also have an external cloaca; Marsupialia derive their name from the term marsupium, meaning pouch, but female echidnas also have a pouch and some marsupial species (e.g., some didelphids) lack a pouch; lastly, Placentalia are named so because of their placenta, but marsupials and monotremes also all have a kind of placenta during pregnancy (as do some fish and lizard species!). Hence, we have to live with the fact that mammals are classified into inappropriately teleological stem-groups (Prototheria, Metatheria and Eutheria) and crown groups with names that are misleading (Monotremata, Marsupialia and Placentalia) but at least we all know what we are talking about. MONOTREMES Then comes a quadruped as big as a large cat, with the eyes, colour, and skin of a mole, and the bill and web-feet of a duck puzzling Dr Shaw, and rendering the latter half of his life miserable, from his utter inability to determine whether it was a bird or a beast... (Smith 1819). At least 180 million years ago even before the dinosaurs had their heyday the prototherian lineage diverged from other mammals (Kemp 2005; Meredith et al. 2011). It has evolved through time without leaving much of a trace, with only one species of platypus and four very similar species of echidna alive today, together with an intriguing but limited fossil record. The platypus (Ornithorhynchus anatinus; family Ornithorhynchidae) is a semi-aquatic creature somewhat resembling otters, but with a duck-like, toothless beak. In fact, its overall appearance is so unusual for mammals that the first specimens sent from Australia to the Natural History Museum in London were considered a masterfully executed hoax (Shaw 1800). The platypus occurs only in eastern Australia and Tasmania, but live in any body of water, from fast-flowing creeks to lakes. Their diet consists mostly of aquatic invertebrates. Echidnas (family Tachyglossidae) are spiny creatures superficially like large hedgehogs. The New Guinean long-beaked echidnas (Zaglossus attenboroughi, bartoni, and bruijni) are fairly large, with adults weighing up to 17 kg (Dawson et al. 1979). They have toothless long snouts adapted for foraging for small invertebrates such as worms and insect larvae. The

6 6 Vera Weisbecker and Robin M. D. Beck Australian short-beaked echidna (Tachyglossus aculeatus) has gone even further and evolved a particular preference for ants and termites (Augee et al. 2006). Monotreme Origins The fossil record of monotremes is extremely sparse but full of tantalising clues. It starts with the question as to where monotremes came from and how they are related to other mammals, both living and extinct (see Box 1). Currently, the most popular hypothesis is that monotremes are the last survivors of an ancient radiation of southern hemisphere mammals called Australosphenida (Luo et al. 2001). This suggestion has been driven by the discovery over the last years of a series of fossil mammals from Australia, South America and Madagascar that appear to be closely related to monotremes (Luo et al. 2001). Interestingly, these fossil mammals exhibit a distinctive, highly complex molar morphology that is known as tribosphenic. Tribosphenic molars allow a complex double function chewing ability, with both shearing and grinding phases (Kemp 2005). For many years, tribospheny was thought to have evolved only once, in the ancestors of Theria (marsupials and placentals; see Box 1) (Bown & Kraus 1979). However, although fossil australosphenidans have tribosphenic molars that appear very similar to those of therians, some key differences suggest that australosphenidan tribosphenic teeth evolved convergently (Luo et al. 2001) - something that would never have been suggested 20 years ago. As part of the australosphenidan radiation, monotremes are almost certainly a Gondwanan group (Luo et al. 2001). Gondwana is an ancient super-continent which was composed of what later became Africa, Madagascar, New Zealand, South America, Antarctica, and Australia. Of these, South America, Antarctica and Australia remained together the longest, sharing a common flora and fauna (Merrick et al. 2006). Antarctica was not the inhospitable, icy continent that it is today, but was covered in temperate rainforest similar to that seen in parts of southern South America and Tasmania (Reguero et al. 2013). After Gondwana broke up the last step being the final separation of Australia from Antarctica as late as 35 million years ago (Lawver et al. 2011) the trans-gondwanan fauna and flora was split, which explains why many South American and Australian animal and plant species are relatively closely related (Merrick et al. 2006). Prototherians are an excellent example of this, with nearly all fossils found to date coming from Australia, except one fossil (the aptly named Monotrematum sudamericanum) found in South America. This suggests that monotremes were once spread across Gondwana but went extinct in South America and Antarctica. Prototherian Evolution The oldest known clearly monotreme-like fossils are fragments of lower jaw, preserving a few teeth, from the Early Cretaceous (around million years ago) of Australia. They belong to the mouse-sized Teinolophos trusleri from Flat Rocks, Victoria, and the much larger (perhaps cat-sized) Steropodon galmani from Lightning Ridge, New South Wales (Kielan-Jaworowska et al. 2004). Other fossils of possible close relatives of living monotremes from this time period are an echidna-like humerus, which has been named

7 Marsupial and Monotreme Evolution and Biogeography 7 Kryoryctes cadburyi, from Dinosaur Cove, Victoria (Pridmore et al. 2005), and Kollikodon ritchiei, also from Lightning Ridge (Flannery et al. 1995). The dentition of K. ritchei is so unusual that its discoverers nearly named it "Hotcrossbunodon" due to the resemblance of the teeth to hot cross buns, (see Long et al. 2002). It was originally described as a monotreme but more recently has been suggested to belong to an entirely different branch of the mammal family tree (Musser 2003; 2013). There is then a gap of approximately 50 million years where no monotreme-like fossils are known. The next oldest fossil and only South American species, Monotrematum sudamericanum, is known from isolated molar teeth and a partial femur. It was found in the early Palaeocene (approx. 64 million years ago) of Patagonia (Pascual et al. 1992). Based on recent studies that have used molecular clocks to estimate when the modern platypus and echidna lineages diverged from each other, Teinolophos, Steropodon, and Monotrematum appear to pre-date this split, and so are probably not members of the monotreme crown-group (Phillips et al. 2009); however, all three are poorly known due to the fragmentary nature of their fossils, and so we can say relatively little about the anatomy and biology of these early monotreme relatives. Box 2. Jaw bones Despite being small enough to easily fit into a matchbox, the jaw fragments of the Early Cretaceous Teinolophos and Steropodon have been the subject of heated debate. Teinolophos in particular has had a controversial history; in 2005, it was claimed that this species still had its middle ear bones attached to the dominant lower jaw bone, the dentary (Rich et al. 2005). This is an ancestral condition where the middle ear bones were still part of the chewing apparatus of the jaw; all living mammals (including monotremes) have the middle ear bones completely detached from the jaw. The existence of this attachment in Teinolophos which was greeted with much scepticism (Bever et al. 2005; Rougier et al. 2005) - would imply that the detachment of the middle ear bones from the jaw occurred independently in the lineage leading to modern monotremes (Prototheria) and the lineage leading to modern marsupials and placentals (Theria). However, shortly after Rowe et al. (2008) suggested that Teinolophos did not have its middle ear bones attached to the jaw after all, and that it was, in fact, a fullyfledged member of the platypus family Ornithorhynchidae as was Steropodon! The idea that members of the modern platypus family existed in the Early Cretaceous, predating previous morphological and molecular estimates by 100 million years, was sensational but short-lived. A follow-up study (Phillips et al. 2009) pointed out that the main character used to place Steropodon and Teinolophos together with the platypus (an enlarged mandibular canal) also exists in echidnas, albeit to a lesser degree (probably because the lower jaw of echidnas is so poorly developed). This study also presented a phylogenetic analysis that firmly placed Teinolophos and Steropodon outside the crown monotremes. An accompanying molecular clock analysis estimated the platypus-echidna divergence as having occurred during the Cenozoic, million years ago (Phillips et al. 2009). After the South American Monotrematum, there is another gap of around 38 million years, until approximately 25 million years ago when we see the first fossils that can probably be referred to as either platypus or echidnas (and so appear to be members of the monotreme crown-group), found at various fossil sites in Australia (Musser 2003; 2013). Of these, the

8 8 Vera Weisbecker and Robin M. D. Beck platypus lineage is much the better documented. In particular, several fossils from the genus Obdurodon give some indication of how the platypus evolved because they have a permanent, functional set of teeth, as well as a platypus-like bony structure to support a beak (Musser & Archer 1998). Four species of Obdurodon are currently known; the oldest species is Obdurodon insignis from the late Oligocene (ca. 25 mya) (Woodburne & Tedford 1975), an undescribed species ("Obdurodon sp. A", Woodburne & Tedford 1975) from the Etadunna formation, followed by Obdurodon dicksoni from the middle Miocene of Riversleigh, Queensland (ca. 15 mya) (Musser & Archer 1998) and lastly the newly-discovered Obdurodon tharalkooschild (5-15 mya) (Pian et al. 2013), which was a giant (perhaps 1 m in length) species also from Riversleigh. The early fossil record of echidnas is exceedingly sparse, probably due to the fact that they have no teeth (they are edentulous ). Teeth are the most common mammal fossils to be preserved, because they are comprised of extremely resilient enamel and dentine. In addition, few skeletal traits are as diagnostic as teeth, so that (for example) fragments of limb bone belonging to an echidna may not be recognised as such. The fossil record of echidnas starts with the giant Megalibgwilia robusta, from deposits that might be as old as the Miocene (although they might be much younger (Musser 2013)). The remainder of the echidna fossil record is from the Pleistocene (probably starting 1.8 mya) and includes the giant Zaglossus hacketti, which could have been up to 1 m long (Long et al. 2002). Box 3. Are echidnas derived from an ancestrally platypus-like monotreme body plan? Through the use of dental characters, it has been possible to draw reasonably well-supported connections between fossil species and living monotremes. The dentition of Teinolophos and Steropodon, for example, closely resembles that of the extinct platypus Obdurodon and the deciduous teeth of juveniles of the modern platypus (Archer et al. 1985; Rich et al. 2001). Similarly, the South American fossil Monotrematum sudamericanum from the Palaeocene (~ 61 mya) is represented by molars that are so much like those of Obdurodon that the species is included by some in the platypus family Ornithorhynchidae (Musser 2013), although others disagree (Phillips et al. 2009). This raises the question as to how the echidna fits in. Some have argued that the echidna may have evolved relatively recently from a platypus-like ancestor (Phillips et al. 2009). This conclusion is supported by the many platypuslike traits seen in echidnas; in particular, echidna locomotion is very platypus-like, they have a vestigial venom spur, and the snout of echidnas is surrounded by a bill-like cartilage in embryos and looks much like a thin, elongated platypus snout in adults (Phillips et al. 2009). In addition, the snout of echidnas is electroreceptive, albeit to a lesser degree than the bill of the platypus (Proske et al. 1998). If this is correct, echidnas may be oddities among monotremes, with the living platypus more representative of the typical morphology of the group. However, it has been pointed out that this conclusion is based on the small handful of fossils available to us (Camens 2010) confident resolution of this question will need to await better sampling of the fossil record. Modern Monotreme Biogeography Despite their ancient heritage and specialized feeding ecology, monotremes are extremely versatile when it comes to ecological conditions. As an aquatic mammal, the platypus is restricted to areas with permanent watercourses that occur along the eastern and southern

9 Marsupial and Monotreme Evolution and Biogeography 9 coast of Australia. The species is now extinct in South Australia, but occurs from Tasmania north to far north Queensland, up to 15 degrees South (Grant 2007). Compared to echidnas, platypus individuals are morphologically quite uniform, although members of southern populations are larger than those of northern ones (Grant 2007). According to Augee et al. (2006), short-beaked echidnas are found in a greater diversity of habitats than any other mammalian species except the house mouse, occurring everywhere from the snowy regions of south-eastern Australia to the tropical lowlands of New Guinea. However, short-beaked echidnas include several morphologically distinct subspecies that are restricted to defined regions that may reflect particular habitats, and these may turn out to be separate species with more detailed study. The subspecies currently recognised are T. a. acanthion from northern Australia, T.a. aculeatus from eastern New South Wales, Victoria, and Southern Queensland, T. a. lawesii from the lowlands of New Guinea and possibly also the rainforests of northeastern Queensland, T.a. multiaculeatus from South Australia, and T. a. setosus from Tasmania (Augee et al. 2006). Long-beaked echidnas (Genus Zaglossus) occur in diverse New Guinean habitats. The four recognised Zaglossus species appear morphologically relatively distinct, and they show biogeographical structuring that may reflect different habitat preferences. Z. bruijnii occurs only in western New Guinea; Z. bartoni occurs in central and western New Guinea (Flannery & Groves 1998). A third species, Z. attenboroughi, is reported to exist in the Cyclops mountains of New Guinea, where a skin was collected in the 1960s (Flannery & Groves 1998). This species may not be a valid taxon and seems to be exceedingly rare, although digging traces and sightings by locals were reported recently (Baillie et al. 2009). The biogeography of long-beaked echidnas has an interesting twist: today, long-beaked echidnas are currently believed to be restricted to New Guinea, but they clearly once also existed across Australia. In fact, Aboriginal rock paintings suggest that they were probably contemporary with humans (Helgen et al. 2012). Until recently, it was assumed that Zaglossus went extinct in Australia sometime in the Pleistocene (before years; (Helgen et al. 2012)). However, researchers recently found a skin in the collections of the Natural History Museum that clearly belonged to Zaglossus, but that had almost certainly been collected in the remote Kimberley region of Western Australia. This means that Zaglossus appears to have existed in Australia into the 20 th century and, given the remoteness of the Kimberley region, it is possible that it still occurs there (Helgen et al. 2012). MARSUPIALS Marsupials are much more diverse and speciose than monotremes, with more than 330 extant species in seven orders (Figure 2). Aside from a few notable exceptions, marsupials have a convergent answer (i.e., an example of independent evolution of a trait) to nearly every placental adaptation: wombats and kangaroos compare to large placental herbivores; the numbat is a marsupial anteater; the marsupial mole is as specialised for digging as are the placental true moles and golden moles; the thylacine (or Tasmanian tiger ), Tasmanian devil and quolls are (or were, in the case of the thylacine) similar to placental carnivores (Flannery 1995; Springer et al. 1997; Van Dyck & Strahan 2008). Various possums share with placental gliding rodents an extensive membrane attached to their limbs to allow gliding, and

10 10 Vera Weisbecker and Robin M. D. Beck caenolestids resemble shrews (Flannery 1995; Springer et al. 1997; Van Dyck & Strahan 2008). Convergence between placentals and marsupials can be extremely far-reaching. For example, the aye-aye, a lemur that extracts grubs from within wood with an extremely thin, elongated middle finger, is very similar to the marsupial striped possums and trioks (species of Dactyopsila and Dactylonax) of New Guinea and northern Queensland, which employ the same grub-catching technique but which use an extremely elongated ring finger (Cartmill 1974; Flannery 1995). Figure 2. A time-calibrated family-level marsupial phylogeny summarising recent studies, including selected fossil crown- and stem-taxa ( ). Family names are at the branch tips, orders are indicated by light grey bars and associated names. Additional relevant clade terms are also added associated with dark grey bars. Estimated divergence dates are from Mitchell et al. (2014), augmented by Beck et al. (unpublished).

11 Marsupial and Monotreme Evolution and Biogeography 11 Also of interest are cases where one marsupial is convergent on several placentals. For example, striped possums and trioks also have black and white stripes and are foul smelling (an experience we have enjoyed when going through drawers of specimens in museums), rather like placental skunks (Flannery 1995). There are also cases where convergence between marsupials and placentals is only partial. For example, the only placentals to feed exclusively on pollen and nectar are various species of flying bat, whereas the only fully nectarivorous marsupial is a non-flying possum, the honey possum or noolbenger (Tarsipes rostratus) (Russell & Renfree 1989; Van Dyck & Strahan 2008). The morphological and ecological diversity of marsupials makes them ideal for comparative study of mammalian ecology and adaptation. This diversity is distributed across seven marsupial orders: three South American and four Australian. How these orders and the families they include are related is shown in Figure 2. The following will provide a brief characterisation in order of presumed evolutionary divergence (which may change with future phylogenetic analyses). For more detailed information on the modern marsupial species, we recommend the comprehensive Animal Diversity Web, a publication of the Museum of Zoology of the University of Michigan: Ameridelphia The term Ameridelphia is often used for a grouping of the South American orders Paucituberculata and Didelphimorphia. However, these two orders probably do not form a clade (see Figure 2), in which case formal use of the name Ameridelphia is inappropriate. It is worth knowing the term, however, since it still often appears in the literature as a shorthand term for South American marsupials excluding Microbiotheria. Didelphimorphia ( True Opossums) Today, the order Didelphimorphia is normally recognised as comprising a single living family, Didelphidae (Voss & Jansa 2009). However, this family is very speciose, with over 100 species described to date (Gardner 2008; Voss & Jansa 2009). More species are described every year, as researchers carry out new fieldwork and also study existing museum specimens

12 12 Vera Weisbecker and Robin M. D. Beck in more detail (often using molecular techniques that were previously unavailable); thus, this total is likely to rise quite considerably (e.g., Voss et al. 2013). Didelphids occur throughout South and Central America (Gardner 2008), but only a single species, the Virginia opossum (Didelphis virginiana) occurs north of Mexico (Voss & Jansa 2009). Based on this modern distribution and their known fossil record, didelphids appear to be an almost exclusively South American radiation (Jansa et al. 2014); the presence of several species in Central America and the Virginia opossum in North America is the result of a relatively recent northward dispersal (Woodburne 2010; Jansa et al. 2014; see also below). Modern didelphids are anatomically relatively conservative, and the overall morphology of their skulls and teeth is probably broadly similar to the last common ancestor of Marsupialia (Voss & Jansa 2009). Body masses of didelphid species range from ~15g (e.g., Kalinowski's mouse opossum, Hyladelphys kalinowskii) to over 6kg (large male specimens of the Virginia opossum). Didelphids can be arboreal (tree-dwelling), scansorial (capable of climbing) or terrestrial, with a single semi-aquatic species, the water opossum or yapok (Chironectes minimus), also known (Gardner 2008). Didelphids also exhibit a range of diets, with woolly opossums (subfamily Caluromyinae) eating a significant proportion of fruit, while some large species, e.g., the lutrine opossum (Lutreolina crassicaudata), regularly eating vertebrate prey; however, most species appear to be predominantly insectivorous or omnivorous (Gardner 2008). Didelphid species in the genus Didelphis (most famously the Virginia opossum) have the ability to play possum, which is a death-feigning reaction in response to threats. In this state, opossums emit a putrid odour and defecate/urinate, which makes their display of being dead all the more convincing. Interestingly, the opossums seem to be conscious during a playing possum episode (Gabrielsen & Smith 1985). Didelphids are the main marsupial representatives in biomedical research because of their great popularity as model organisms, particularly the grey short-tailed opossum (Monodelphis domestica) (Selwood & Coulson 2006). It is possible that the mistaken impression that marsupials are small-brained compared to placentals stems from the fact that the well-studied Virginia opossum has a particularly small brain relative to its body size (Weisbecker & Goswami 2010). Paucituberculata (Shrew Opossums) This elusive order only contains one living family, Caenolestidae, which has seven species in three genera (Caenolestes, Rhyncholestes, and Lestoros). However, the extensive fossil record shows that Paucituberculata were once a diverse group of marsupials with several additional families known (Abello 2013). Modern caenolestids are small (<50g), mostly insectivorous animals whose ecology is little understood (Gardner 2008), and new species continue to be described (e.g., Ojala-Barbour et al. 2013). Australidelphia (Microbiotheria and Australian and New Guinean Species) Microbiotheria (Monito del Monte) Today, there is a single living member of the marsupial order Microbiotheria, the monito del monte ( little monkey of the mountains in Spanish), Dromiciops gliroides. The monito del monte lives in temperate rainforest and bamboo thickets in southern South America. The

13 Marsupial and Monotreme Evolution and Biogeography 13 size of a mouse (~25g), this species is arboreal and primarily insectivorous, but also eats some fruit (Gardner 2008). The taxonomic history of microbiotherians is complicated, and the order plays a central role in our current understanding of marsupial phylogeny and biogeography. The first microbiotherian to be described was actually a fossil species, Microbiotherium patagonicum. It was named by the great early palaeontologist Florentino Ameghino in 1887, based on specimens from ~17 million year (Ma) old rocks in Patagonia, southern Argentina (Ameghino 1887). The name of the species means short-lived mammal from Patagonia, reflecting Ameghino s belief that it was a member of a group that was entirely extinct. Seven years later, the eminent mammologist Michael Oldfield Thomas described the extant species, Dromiciops gliroides, and identified it as a didelphid (Thomas 1894). In 1955, Osvaldo Reig first proposed that Dromiciops was in fact a living relative of Microbiotherium (Reig 1955). Nevertheless, most researchers, including Reig himself, continued to assume that Dromiciops and Microbiotherium were just slightly odd didelphids. However, in 1982, the palaeontologist Fred Szalay made the revolutionary suggestion that Dromiciops and Microbiotherium are not didelphids, but are in fact more closely related to Australian marsupials (Szalay 1982). As discussed in more detail below, the evidence in favour of Szalay s hypothesis is now overwhelming, and Dromiciops, Microbiotherium and fossil relatives are therefore now assigned to their own order, Microbiotheria. The fossil record of microbiotherians is restricted to South America and the fringes of Antarctica (Reguero et al. 2013). Dasyuromorpha (Australian Carnivorous Marsupials) Dasyuromorphia include >70 species in three families - Dasyuridae, Myrmecobiidae (the ant-eating numbat), and Thylacinidae (the extinct thylacine or Tasmanian tiger ). Most species are quite small, such as the tiny antechinuses and dunnarts, but they also include the slightly larger phascogales, the cat-sized quolls, as well as the famous Tasmanian devil and thylacine, which represent the largest modern dasyuromorphians (Flannery 1995; Van Dyck & Strahan 2008).

14 14 Vera Weisbecker and Robin M. D. Beck Myrmecobiidae and Thylacinidae comprise a single modern species each, but several thylacinid species are known from the fossil record (Wroe 2003). The family Dasyuridae, by contrast, is highly diverse today. It includes the smallest known marsupial, the ~4g long-tailed planigale (Planigale ingrami) and the largest living carnivorous marsupial, the ~8kg Tasmanian devil (Sarcophilus harrisii). All dasyurid species mainly feed on animal prey and even the smallest members of the clade (such as planigales) will attack vertebrate prey such as lizards or small birds (Van Dyck & Strahan 2008). Most dasyurids are terrestrial, although many are capable of climbing, and phascogales (Phascogale spp.) are predominantly arboreal (Van Dyck & Strahan 2008). Dasyurids inhabit all Australian habitats, including some of the harshest desert regions, as well as the high Australian and New Guinean tropics (Van Dyck & Strahan 2008). Several dasyurid species, including species of Antechinus, Dasykaluta, Phascogale, Parantechinus and Dasyurus, have evolved the striking trait of semelparity, where males mate only once in their lifetime and die off shortly afterwards. It seems that this type of reproduction allows males to produce the best quality sperm possible, which increases their chances of siring offspring (Fisher et al. 2013). Interestingly, semelparity of males has also been described in several didelphid species; in a few of these, the adult females also die after weaning their offspring (Lopes & Leiner 2015). However, semelparity has never been observed in placentals or monotremes, and so it is possible that some aspect of marsupial biology favours the evolution of this reproductive strategy, which is otherwise rare in vertebrates. Thylacines and Tasmanian devils survived on mainland Australia and New Guinea until a few thousand years ago, but became extinct there prior to European arrival. The disappearance of the thylacine and also the Tasmanian Devil from mainland Australia ~3000 years ago has been linked to the arrival of the dingo at this time, but this remains controversial (Letnic et al. 2012). Both the thylacine and the devil survived on Tasmania, where the dingo is absent. The devil managed to survive to the present day, but the thylacine succumbed to a concerted eradication effort, although its real impact on livestock remains unclear (a famous photograph of a thylacine carrying a chicken is probably staged using a stuffed thylacine skin; Freeman 2005)); the devil is now protected but is currently severely threatened by the devil facial tumour disease, an infectious cancer which kills affected individuals through the rampant growth of a facial tumour (McCallum et al. 2007). Peramelemorphia Today, the order Peramelemorphia comprises of two families: Thylacomyidae, with a single living species, the greater bilby (Macrotis lagotis), and Peramelidae, the bandicoots, with 19 described species. However, ongoing collecting and taxonomic revisions mean that

15 Marsupial and Monotreme Evolution and Biogeography 15 several more bandicoot species are likely be described in the future, particularly from the more inaccessible regions of New Guinea (Helgen & Flannery 2004; Westerman et al. 2012). Multiple fossil bandicoot species are also known, many of which fall outside the crown-group (Travouillon et al. 2013). A number of bandicoot species have gone extinct within the last 150 years or so, including the lesser bilby (Macrotis leucura) and the pig-footed bandicoot (Chaeropus ecaudatus), which was the only known representative of the family Chaeropodidae (Jones 1923). The pig-footed bandicoot was remarkable because it had modified its forefeet into hoof-like structures (Jones 1923). Hooves have evolved multiple times among placentals but no other known marsupial has hooves, perhaps because of constraints on the morphology of their forelimbs due to the need for neonates to crawl to the mother s nipple (see Chapter 11). Exactly how the pig-footed bandicoot overcame this presumed constraint is unknown, and may never be resolved now that the species is extinct. All living peramelemorphians are omnivorous, with the greater bilby more herbivorous (Van Dyck & Strahan 2008). The greater bilby is a nocturnal species found in arid Australia, which keeps cool in relatively complex burrows (Van Dyck & Strahan 2008). Their rabbitlike appearance and half-bounding locomotion has led to its use as a native alternative to the European Easter Bunny (rabbits being destructive pests in Australia, and having replaced bilbies in many places; Lees & Bell 2008)). Bandicoots range in size from <100g (Microperoryctes spp.) to ~5kg (males of Peroryctes broadbenti), and are distributed across Australia and New Guinea, with different species occurring in wet rainforest and arid environments (Flannery 1995; Van Dyck & Strahan 2008). This, as well as their high rate of reproduction, has made them quite resilient to human-induced disturbances (Scott et al. 1999). In fact, dense cover of introduced weeds such as blackberry brambles and gorse seem to allow some Australian species to stay safe from introduced placental predators (Paull 1995). Notoryctemorphia This order includes two very similar marsupial mole species - Notoryctes typhlops (the southern marsupial mole, or itjaritjari) and N. caurinus (the northern marsupial mole, or

16 16 Vera Weisbecker and Robin M. D. Beck kakarratul) - which live in the deserts of central and western Australia (Van Dyck & Strahan 2008). Marsupial moles are small (~50g) mammals that externally look very similar to the placental golden moles, lacking external ears and with vestigial eyes covered by skin (Stirling 1891; Lees & Bell 2008). Internally, the marsupial mole skeleton is highly modified for digging, with a heavily fused skull and massive muscle attachment sites on their fore- and hindlimbs (Warburton 2006). It used to be thought that marsupial moles swim through sand without creating tunnels, but more recent research has shown that they do create tunnels but backfill them as they go (Benshemesh 2014). Marsupial moles are capable of very rapid digging the first British settlers lost one of the first specimens because they had decided to put it on the ground to see how it dug, and it promptly disappeared at such speed that they could not retrieve it (Stirling 1891)! Diprotodontia The Australian and New Guinean order Diprotodontia is a mammalian clade of superlatives. It is the largest and most speciose marsupial order, containing 11 families and approximately 150 living species (Reeder et al. 2007); however, new species continue being discovered, particularly in New Guinea (Reeder et al. 2007). Diprotodontia is anatomically and ecologically highly diverse, and includes wombats (Vombatidae), koalas (Phascolarctidae), three families of kangaroos and wallabies (Hypsiprymnodontidae, Macropodidae and Potoroidae), and six families of possums (Acrobatidae, Burramyidae, Petauridae, Pseudocheiridae, Phalangeridae and Tarsipedidae). Their unusual diversity also harbours the greatest size range of all mammalian orders (Sánchez-Villagra et al. 2003): the smallest diprotodontian, Tarsipes rostratus, weighs only 7 g, while the largest known species, Diprotodon optatum (which became extinct within the last 50 thousand years), would probably have weighed nearly 3 tons (Wroe et al. 2004).

17 Marsupial and Monotreme Evolution and Biogeography 17 Diprotodontia are mostly herbivores or omnivores (Flannery 1995; Van Dyck & Strahan 2008). However, there are some notable but unfortunately extinct exceptions to this general rule of herbivory. One of the world s largest ever mammalian carnivores was the marsupial lion (Thylacoleo carnifex), a relative of wombats and koalas with tremendous claws and a dentition consisting of a pair of chisel-like incisors and giant shearing premolars (Archer 1984a). The fossil propleopine kangaroos may also have been carnivorous (Wroe et al. 1998). Koalas are also notable feeding specialists who feed nearly exclusively on eucalypt leaves (Van Dyck & Strahan 2008). In addition, diprotodontians are biomedically relevant because the tammar wallaby (Macropus eugenii) is a well-established model organism for biomedical research (Selwood & Coulson 2006). Evolutionary History and Biogeography of Metatheria and Marsupialia The oldest fossil that we can confidently identify as related to modern marsupials is Sinodelphys szalayi, which is approximately 125 million years old the Early Cretaceous - and comes from what might seem like a surprising place: northeastern China (Luo et al. 2003)! Phylogenetic analyses place Sinodelphys within Metatheria but outside Marsupialia (Luo et al. 2003; Luo et al. 2011; see Figure 2). The oldest eutherian is even older than Sinodelphys: the ~160 million year old Juramaia sinensis, also from China. Juramaia implies that Eutheria and Metatheria split at least 160 million years ago (Luo et al. 2011), while some molecular clock studies suggest an even earlier split (Meredith et al. 2011). Fossils of metatherians are known from the Middle and Late Cretaceous (~ million years ago) of Asia, Europe and North America. During the Late Cretaceous (~86-66 million years ago), metatherians were particularly diverse in North America, where they were more common than eutherians (Cifelli & Davis 2003; Williamson et al. 2014). They included fruit-eating and carnivorous forms, and one group (the stagodontids) may have been semi-aquatic (Williamson et al. 2014). However, like nearly all mammals from the Age of Dinosaurs, they were small, with the largest only ~2 kg (Williamson et al. 2014). Also, none of these Cretaceous metatherians from the northern hemisphere appear to be marsupials, but are instead metatherian stem-taxa (see above and Figure 2). The obvious question, then, is what was going on in South America and Australia at this time. The fossil record of Cretaceous mammals in Australia is very poor, but nevertheless there is no trace of metatherians; instead, as discussed above, monotremes (e.g., Teinolophos, Steropodon), other australosphenidans (e.g., Ausktribosphenos, Bishops) and a few other obscure groups were present (Long et al. 2002; Kielan-Jaworowska et al. 2004). The South American fossil record is better, particularly during the Late Cretaceous, but again metatherians have not been found (Kielan-Jaworowska et al. 2004). The simplest explanation

18 18 Vera Weisbecker and Robin M. D. Beck for these observations is that metatherians were genuinely absent from the southern hemisphere at this time. Later, around million years ago, a landbridge or island chain formed between North America and South America (Ortiz-Jaureguizar & Pascual 2011). Several different vertebrate groups moved along this connection, from North America and into South America, including metatherian and eutherian mammals (Muizon & Cifelli 2001), duck-billed dinosaurs (Prieto-Marquez 2010) and alligators (Brochu 2011). Metatherians suffered severely in the KPg mass extinction event 66 million years ago, with only a single species present in the North American fossil record immediately after the KPg boundary, compared to 11 immediately before it (Williamson et al. 2014). Metatherians survived in the northern hemisphere for another 50 million years or so, but remained restricted to smallbodied, insectivorous-omnivorous niches (Crochet 1980; Korth 2008), whereas placentals diversified enormously (Rose 2006). It is in the southern hemisphere that metatherians had their real success story. The oldest metatherians from South America are about 64 million years old, and are already fairly diverse (Muizon and Cifelli 2001). They radiated widely into a range of ecological niches, mostly insectivorous-omnivorous, but also included such animals as the carnivorous sparassodonts, the rodent-like, possibly hopping (Szalay 1994) argyrolagids, and Groeberia, which might have been a (non-flying) mammalian equivalent of a parrot (Goin et al. 2012)! In contrast to Australia, however, in South America eutherians filled the large-bodied herbivorous mammal niches: the so-called South American native ungulates (Goin et al. 2012). The oldest marsupials (i.e., members of the crown-group) from South America are ~50 million years old (Woodburne et al. 2014). However, living didelphids represent a relatively modern radiation, with recent molecular clock studies suggesting that they last shared a common ancestor million years ago (Meredith et al. 2011; Jansa et al. 2014). These studies suggest that extant caenolestids diverged from each other even more recently, 7-15 million years ago (Meredith et al. 2011). From about 9-10 million years ago onwards, mammals began to disperse between North and South America, a process that intensified with the appearance of a permanent landbridge, the Isthmus of Panama, connecting the two continents (Woodburne 2010). This exchange of faunas, termed the Great American Biotic Interchange saw some didelphids moving into Central and North America (Jansa et al. 2014), although only the Virginia opossum managed to colonise the region of North America north of Mexico (Hall 1981). The next question is then, how did marsupials reach Australia? As with monotremes, the existence of Gondwana the ancient super-continent that connected, among others, South America, Antarctica and Australia plays a key role in understanding this question. In fact, marsupials appear to have spread from South America to Australia via Antarctica (Beck et al. 2008; Beck 2012), which was ice-free and connected to South America and Antarctica until about 35 million years ago (Beck et al. 2008; Beck 2012; Reguero et al. 2013; see above). This trans-antarctic dispersal route is plausible because we know that several marsupials and possibly other metatherians made it from South America to Antarctica: their fossils have been found in the 45 million year old La Meseta fauna on Seymour Island, off the coast of the Antarctic Peninsula (Reguero et al. 2013). By the time Gondwana broke up, perhaps as late as million years ago (Lawver et al. 2011), marsupials had already reached Australia: the oldest known marsupial fossils from Australia are 55 million years old, from the Tingamarra fauna in southeastern Queensland (Godthelp et al. 1992). These fossils are highly fragmentary, but at least two are definitely marsupials: Djarthia murgonensis (represented by teeth, jaws, and small fragments of the skull and skeleton) and an isolated ankle bone of