American Marsupials Research Articles

Características Morfológicas de un Grupo de Zarigüeyas (Didelphys marsupialis) del Suroccidente Colombiano

La familia Didelphidae representa la mayoría de los marsupiales americanos ampliamente distribuidos en América del Sur, ocupando casi todo tipo de hábitats a excepción de zonas altas y zonas desérticas. Los marsupiales de la familia varían de tamaño y algunos autores los describen como medianos y grandes, mientras que otros los describen de tamaño pequeño y mediano. El presente trabajo aporta una descripción morfológica de las zarigüeyas ubicadas en una región del suroccidente colombiano.

Mammals from 'down under': a multi-gene species-level phylogeny of marsupial mammals (Mammalia, Metatheria).

Marsupials or metatherians are a group of mammals that are distinct in giving birth to young at early stages of development and in having a prolonged investment in lactation. The group consists of nearly 350 extant species, including kangaroos, koala, possums, and their relatives. Marsupials are an old lineage thought to have diverged from early therian mammals some 160 million years ago in the Jurassic, and have a remarkable evolutionary and biogeographical history, with extant species restricted to the Americas, mostly South America, and to Australasia. Although the group has been the subject of decades of phylogenetic research, the marsupial tree of life remains controversial, with most studies focusing on only a fraction of the species diversity within the infraclass. Here we present the first Methaterian species-level phylogeny to include 80% of the extant marsupial species and five nuclear and five mitochondrial markers obtained from Genbank and a recently published retroposon matrix. Our primary goal is to provide a summary phylogeny that will serve as a tool for comparative research. We evaluate the extent to which the phylogeny recovers current phylogenetic knowledge based on the recovery of “benchmark clades” from prior studies—unambiguously supported key clades and undisputed traditional taxonomic groups. The Bayesian phylogenetic analyses recovered nearly all benchmark clades but failed to find support for the suborder Phalagiformes. The most significant difference with previous published topologies is the support for Australidelphia as a group containing Microbiotheriidae, nested within American marsupials. However, a likelihood ratio test shows that alternative topologies with monophyletic Australidelphia and Ameridelphia are not significantly different than the preferred tree. Although further data are needed to solidify understanding of Methateria phylogeny, the new phylogenetic hypothesis provided here offers a well resolved and detailed tool for comparative analyses, covering the majority of the known species richness of the group.

Intraspecific variability inLestoros inca(Paucituberculata, Caenolestidae), with reports on dental anomalies and eruption pattern

Abstract Caenolestids are a group of poorly known South American marsupials with a restricted distribution in paramo and subparamo environments of the Andes from Colombia and western Venezuela to Bolivia (represented by the genera Caenolestes and Lestoros), and in Valdivian rain forest in southern Chile and Argentina where a single species (Rhyncholestes raphanurus) lives. The Incan shrew opossum, Lestoros inca, lives in mountains of southern Peru and extreme northwestern Bolivia. Despite being common in trapping surveys, little is known of its cranial and dental intraspecific variability, tooth eruption pattern, and dental anomalies. The objective of this work was to analyze the intraspecific variability of L. inca, which includes an anatomical description of the skull and dentition and analysis of clinal variation, tooth eruption patterns, and dental anomalies. The eruption pattern found in L. inca confirms the sequence P3 → m4 → p3 → M4 as the general pattern for living paucituberculatans. Missing teet...

Analysis of dental homologies and phylogeny of Paucituberculata (Mammalia: Marsupialia)

The Paucituberculata is an endemic group of South American marsupials, recorded from the early Cenozoic up to the present. In this report, the most comprehensive phylogenetic analysis of Paucituberculata to date is presented. Fifty-seven terminal species were scored for 74 new and re-examined characters. Homologies of dental characters used in previous systematic studies were critically reviewed to evaluate their inclusion in the analysis. Phylogenetic results corroborated two major paucituberculatan clades, Palaeothentoidea and Caenolestoidea, and the main palaeothentoid groupings: Pichipilidae, Palaeothentidae, and Abderitidae. Taxon sampling and reinterpretations of molar cusp and crest homologies played an important role in the generation of new phylogenetic hypotheses. The main differences with respect to previous phylogenies were focused on palaeothentoid relationships: Palaeothentes boliviensis and Pilchenia lucina are not members of Palaeothentidae but instead clustered with Pilchenia intermedia and P. antiqua, forming the sister-group of a Palaeothentidae + Abderitidae clade, and Titanothentes simpsoni, previously considered a palaeothentine, is nested within the Acdestinae clade. Based on the time-calibrated phylogeny, the following stages in the paucituberculatan evolutionary history are suggested: origin of the group, in the Paleocene to early Eocene at the latest, split of Caenolestoidea and Palaeothentoidea clades during the late early to middle Eocene, evolutionary radiation of palaeothentid and abderitid lineages near the Oligocene–Eocene boundary, and decreased diversity and extinction of palaeothentoids during the middle Miocene. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 441–465.

Revision of the family Listropsoralgidae Fain, 1965 (Acariformes: Sarcoptoidea)—skin parasites of marsupials and rodents

The family Listropsoralgidae Fain, 1965 (Acariformes: Sarcoptoidea) is represented by the permanent skin ectoparasites associated with the South American and Australian marsupials (12 species) and the South American rodents of the family Echimyidae (1 species). The phylogenetic relationships of these mites (12 ingroup and 2 outgroup species) are reconstructed on the basis of the maximum parsimony (MP) and Bayesian analyses (BA) of 76 morphological characters. MP analysis confirmed monophyly of the listropsoralgid genera, the strict consensus of 18 trees generated by MP has the following pattern: Petauralges (Listropsoralgoides, Didelphialges, Listropsoralges) with poor resolution among species of the genus Listropsoralges. The same tree was generated by BA. Both successive and implied weighting strategies resulted in 7 MP trees: Petauralges (Listropsoralgoides (Didelphialges (Listropsoralges))). The relationships between species of the genus Listropsoralges received the poorest resolution: L. caenolestes (L. monodelphis, L. vossi, L. faini, L. brevisetosa (L. thylamys (L. marmosa-L. caluromys))). The host-parasite relationships of listropsoralgids are briefly discussed. The family Listropsoralgidae is taxonomically revised and to date includes 13 species in 4 genera. Six species and one genus are described as new: Listropsoralges brevisetosus sp. n. from Marmosa murina (Didelphimorphia: Didelphidae) from Peru, Listropsoralges similis sp. n. from Caluromys derbianus (Didelphidae) from Panama, Listropsoralges thylamys sp. n. from Thylamys venustus (Didelphidae) from Bolivia, Listropsoralges vossi sp. n. from Monodelphis domestica (Didelphidae) from Brazil, Listropsoralges caenolestes sp. n. from Caenolestes fuliginosus (Paucituberculata: Caenolestidae) from Ecuador, and Didelphialges metachirus gen. n., sp. n. from Metachirus nudicaudatus (Didelphidae) from Peru. The female of Listropsoralges faini Bochkov and Wauthy, 2009 is described for the first time.

An ‘ameridelphian’ marsupial from the early Eocene of Australia supports a complex model of Southern Hemisphere marsupial biogeography

Recent molecular data strongly support the monophyly of all extant Australian and New Guinean marsupials (Eomarsupialia) to the exclusion of extant South American marsupials. This, together with available geological and fossil evidence, has been used to argue that the presence of marsupials in Australia is simply the result of a single dispersal event from South America during the latest Cretaceous or Palaeocene, without subsequent dispersals between the two continents. Here, I describe an isolated ankle bone (calcaneus) of a metatherian from the early Eocene Tingamarra Local Fauna in northeastern Australia. Strikingly, this specimen, QM F30060, lacks the 'continuous lower ankle joint pattern' (CLAJP), presence of which is a highly distinctive apomorphy of the marsupial clade Australidelphia, which includes Eomarsupialia, the living South American microbiotherian Dromiciops and the Tingamarran fossil marsupial Djarthia. Comparisons with a range of marsupials and stem-metatherians strongly suggest that the absence of the CLAJP in QM F30060 is plesiomorphic, and that this specimen represents the first unequivocal non-australidelphian ('ameridelphian') metatherian known from Australia. This interpretation is confirmed by phylogenetic analyses that place QM F30060 within (crown-group) Marsupialia, but outside Australidelphia. Based on these results, the distribution of marsupials within Gondwana cannot be explained by simply a single dispersal event from South America and Australia. Either there were multiple dispersals by marsupials (and possibly also stem-metatherians) between South America and Australia, in one or both directions, or, alternatively, there was a broadly similar metatherian fauna stretching across southern South America, Antarctica and Australia during the Late Cretaceous-early Palaeogene.

Absence of mammary development in maleDromiciops gliroides: another link to the Australian marsupial fauna

The South American microbiotherian marsupial Dromiciops gliroides is regarded as a sister taxon to the monophyletic Australasian marsupial clade. Mammary anlagen have been documented in male American marsupials but have not been observed in males of any Australian marsupials. The aim of this study was to determine if mammary anlagen were present in developing pouch young (PY) of Dromiciops. The developmental anatomy, particularly the presence of mammary anlagen, was investigated in 3 neonatal male (n 5 2) and female (n 5 1) Dromiciops PY (,15–20 days postpartum). External and internal structures were examined to confirm PY gender and to provide basic information on development, particularly of the genitourinary system. In the female PY early pouch development was observed as well as 4 clearly defined abdominal mammary anlagen. No external teat or mammary anlagen development was seen in the 2 male PY and serial sections from the external genitalia to upper thorax failed to reveal any histological structures similar to mammary anlagen seen in the female. Absence of mammary anlagen in male Dromiciops PY provides further evidence that Dromiciops shares a closer relationship with the Australasian marsupial clade than with the American marsupial fauna.

Relationships of South American marsupials (Didelphimorphia, Microbiotheria and Paucituberculata) and hard ticks (Acari: Ixodidae) with distribution of four species of Ixodes

Relationships of South American marsupials (Didelphimorphia, Microbiotheria and Paucituberculata) and hard ticks (Acari: Ixodidae) with distribution of four species of Ixodes

Relationships of South American marsupials (Didelphimorphia, Microbiotheria and Paucituberculata) and hard ticks (Acari: Ixodidae) with distribution of four species of Ixodes

Historical information shows that South American marsupials are irrelevant hosts for South American hard ticks (Ixodidae Murray) of the genera Haemaphysalis Koch, Rhipicephalus Koch and Dermacentor Koch. Twenty two Amblyomma Koch species were occasionally found on Didelphimorphia Gill, but some records are doubtful (i.e., A. dissimile Koch, 1844) and only A. fuscum Neumann, 1907 appears to be a relevant parasite of this type of host. Twelve species of Ixodes Latreille were determined on these hosts, although one of them, I. longiscutatus Boero, 1944, is probably misidentified. Four species, I. amarali Fonseca, 1935b, I. loricatus Neumann, 1899, I. luciae Sénevet, 1940 and I. venezuelensis Kohls, 1953 are usual parasites of Didelphimorphia. These species (I. venezuelensis excluded) have adult ticks feeding mostly on Didelphidae Gray, and sub-adult ticks feeding mostly on Didelphidae and several species of sigmodontine rodents. All parasitic stages of I. venezuelensis were recorded from Didelphimorphia although rodents are also of importance for its life cycle. Records from marsupials and nonmarsupial hosts show that I. amarali is established in eastern Brazil, and I. venezuelensis in Venezuela, Colombia, Panama and Costa Rica. The alleged southernmost record of I. luciae in Central Argentina was found to be erroneous and its southern limit is located in northwestern Argentina and its way northwards includes Bolivia, Peru, western Brazil, French Guiana, Surinam, Trinidad & Tobago, Panama, Guatemala, Belize and southern Mexico with unconfirmed but probably valid records for Ecuador, Colombia, Costa Rica, Nicaragua and Honduras. The distribution of I. loricatus has been historically considered to range from southern Argentina to southern Mexico but southernmost and northernmost records are now considered doubtful along with Venezuelan populations for this tick, while the only records for Panama and Colombia were based on wrong tick identifications. Bona fide populations of I. loricatus range from central-eastern Argentina and southern Uruguay to Paraguay up to north-eastern Brazil. Dromiciops gliroides Thomas, the only member of Microbiotheria Ameghino is the exclusive host of Ixodes neuquenensis Ringuelet, 1947. There is only one record of tick infestation (Ixodes jonesae Kohls, Sonenshine & Clifford, 1969) of Paucituberculata Ameghino, indicating that these marsupials are of no apparent importance for maintenance of South American hard ticks. We speculate that the species of Ixodes feeding on Didelphimorphia and Sigmodontinae Wagner are a clade derived from ancestors feeding exclusively on Didelphidae that radiated after the invasion of South America by Sigmodontinae or their ancestors. Ixodes neuquenensis (established in south-western South America) is considered a relatively new species that radiated from Ixodes parasites of Sigmodontinae invaders in southern South America.

The tammar wallaby major histocompatibility complex shows evidence of past genomic instability.

BackgroundThe major histocompatibility complex (MHC) is a group of genes with a variety of roles in the innate and adaptive immune responses. MHC genes form a genetically linked cluster in eutherian mammals, an organization that is thought to confer functional and evolutionary advantages to the immune system. The tammar wallaby (Macropus eugenii), an Australian marsupial, provides a unique model for understanding MHC gene evolution, as many of its antigen presenting genes are not linked to the MHC, but are scattered around the genome.ResultsHere we describe the 'core' tammar wallaby MHC region on chromosome 2q by ordering and sequencing 33 BAC clones, covering over 4.5 MB and containing 129 genes. When compared to the MHC region of the South American opossum, eutherian mammals and non-mammals, the wallaby MHC has a novel gene organization. The wallaby has undergone an expansion of MHC class II genes, which are separated into two clusters by the class III genes. The antigen processing genes have undergone duplication, resulting in two copies of TAP1 and three copies of TAP2. Notably, Kangaroo Endogenous Retroviral Elements are present within the region and may have contributed to the genomic instability.ConclusionsThe wallaby MHC has been extensively remodeled since the American and Australian marsupials last shared a common ancestor. The instability is characterized by the movement of antigen presenting genes away from the core MHC, most likely via the presence and activity of retroviral elements. We propose that the movement of class II genes away from the ancestral class II region has allowed this gene family to expand and diversify in the wallaby. The duplication of TAP genes in the wallaby MHC makes this species a unique model organism for studying the relationship between MHC gene organization and function.

Observations on the captive behavior of the rare Patagonian opossum Lestodelphys halli (Thomas, 1921) (Marsupialia, Didelphimorphia, Didelphidae)

We describe the behavior in captivity of the rare Patagonian opossum (Lestodelphys halli) from five individuals captured at three localities, which were kept alive in glass terraria for different periods of time (between 2.5–3.5 months). During our observations we found that L. halli can climb and jump well, has a prehensile tail-tip which can hold the body suspended for several seconds, powerful grasping hind feet and the ability to dig. Feeding preferences of meat (mainly raw) and live animals (i.e., mice, lizards and beetles) over vegetables or fruit was observed. We document the first records of torpor/hibernation for the species, its locomotion and exploration patterns and feeding postures. Resting/sleeping in L. halli is done with the body curled along a vertical axis and its head placed against the chest and between the hind legs, a posture different from previously reported American marsupials. Stereotyped behavior patterns (e.g., grooming) were observed and compared with other studied species, providing comparative information for further studies on New World marsupials.

Tracking Marsupial Evolution Using Archaic Genomic Retroposon Insertions

Author SummaryEver since the first Europeans reached the Australian shores and were fascinated by the curious marsupials they found, the evolutionary relationships between the living Australian and South American marsupial orders have been intensively investigated. However, neither the morphological nor the more recent molecular methods produced an evolutionary consensus. Most problematic of the seven marsupial groups is the South American species Dromiciops gliroides, the only survivor of the order Microbiotheria. Several studies suggest that Dromiciops, although living in South America, is more closely related to Australian than to South American marsupials. This relationship would have required a complex migration scenario whereby several groups of ancestral South American marsupials migrated across Antarctica to Australia. We screened the genomes of the South American opossum and the Australian tammar wallaby for retroposons, unambiguous phylogenetic markers that occupy more than half of the marsupial genome. From analyses of nearly 217,000 retroposon-containing loci, we identified 53 retroposons that resolve most branches of the marsupial evolutionary tree. Dromiciops is clearly only distantly related to Australian marsupials, supporting a single Gondwanan migration of marsupials from South America to Australia. The new phylogeny offers a novel perspective in understanding the morphological and molecular transitions between the South American and Australian marsupials.

Molecular characterization of an ancient Hepatozoon species parasitizing the ‘living fossil’ marsupial ‘Monito del Monte’ Dromiciops gliroides from Chile

The Microbiotheriid Dromiciops gliroides, also known as ‘Monito del Monte’, is considered to be a threatened species and the only living representative of this group of South American marsupials. During the last few years, several blood samples from specimens of ‘Monito del Monte’ captured at Chiloe island in Chile have been investigated for blood parasites. Inspection of blood smears detected a Hepatozoon species infecting red blood cells. The sequences of DNA fragments corresponding to small subunit ribosomal RNA gene revealed two parasitic lineages belonging to Hepatozoon genus. These parasite lineages showed a basal position with respect to Hepatozoon species infecting rodents, reptiles, and amphibians but are phylogenetically distinct from Hepatozoon species infecting the order Carnivora. In addition, the Hepatozoon lineages infecting D. gliroides are also different from those infecting other micro-mammals living in sympatry, as well as from some that have been described to infect an Australian species of bandicoot. The potential vector of this parasite appears to be the host-specific tick Ixodes neuquenensis because the sequencing of a long amplicon determined the presence of one of the two lineages found in the marsupial. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 568–576.

Abdominal muscle and epipubic bone function during locomotion in Australian possums: Insights to basal mammalian conditions and eutherian‐like tendencies in Trichosurus

Mammals have four hypaxial muscle layers that wrap around the abdomen between the pelvis, ribcage, and spine. However, the marsupials have epipubic bones extending anteriorly into the ventral hypaxial layers with two additional muscles extending to the ventral midline and femur. Comparisons of South American marsupials to basal eutherians have shown that all of the abdominal hypaxials are active bilaterally in resting ventilation. However, during locomotion marsupials employ an asymmetrical pattern of activity as the hypaxial muscles form a crosscouplet linkage that uses the epipubic bone as a lever to provide long-axis support of the body between diagonal limb couplets during each step. In basal eutherians, this system shifts off the femur and epipubic bones (which are lost) resulting in a shoulder to pelvis linkage associated with shifts in both the positions and activity patterns of the pectineus and rectus abdominis muscles during locomotion. In this study, we present data on hypaxial function in two species (Pseudocheirus peregrinus and Trichosurus vulpecula) representing the two major radiations of possums in Australia: the Pseudocheiridae (within the Petauroidea) and the Phalangeridae. Patterns of gait, motor activity, and morphology in these two Australian species were compared with previous work to examine the generality of 1) the crosscouplet lever system as the basal condition for the Marsupialia and 2) several traits hypothesized to be common to all mammals (hypaxial tonus during resting ventilation, ventilation to step synchrony during locomotion, and bilateral transversus abdominis activity during locomotor expiration). Our results validate the presence of the crosscouplet pattern and basic epipubic bone lever system in Australian possums and confirm the generality of basal mammalian patterns. However, several novelties discovered in Trichosurus, reveal that it exhibits an evolutionary transition to intermediate eutherian-like morphological and motor patterns paralleling many other unique features of this species.

Chulpasia and Thylacotinga, late Paleocene-earliest Eocene trans-Antarctic Gondwanan bunodont marsupials: New data from Australia

A new marsupial from the early Eocene Tingamarra Local Fauna of southeastern Queensland, Australia, is named and referred to Chulpasia Crochet and Sigé, 1993, a genus otherwise known from early Tertiary deposits of Peru. This taxon, Chulpasia jimthorselli nov. sp., differs in upper molar morphology only in minor details from the Peruvian type species Chulpasia mattaueri and is almost identical in size. New materials referable to the Tingamarra marsupial Thylacotinga bartholomaii Archer, Godthelp and Hand are also described. Species of Chulpasia and Thylacotinga share many striking derived as well as plesiomorphic dental features that allow recognition of a new monophyletic subfamily, Chulpasiinae. Its familial relationships are in doubt, but members of the subfamily could have provided the ancestral stock for Rosendolops and other early Tertiary South American polydolopimorphian marsupials. This is the first evidence that a Gondwanan genus of therian land mammals spanned South America, Antarctica and Australia during the early Tertiary. The very close similarity between the Peruvian and Australian fossils (and suggested short time span between their stratigraphic occurrences) provides further paleontological support for a trans-Antarctic land connection between South America and Australia extending well into the early Paleogene.

American marsupials chromosomes: why study them?

Marsupials, one of the three main groups of mammals, are only found in Australia and in the American continent. Studies performed in Australian marsupials have demonstrated the great potential provided by the group for the understanding of basic genetic mechanisms and chromosome evolution in mammals. Genetic studies in American marsupials are relatively scarce and cytogenetic data of most species are restricted to karyotype descriptions, usually without banding patterns. Nevertheless, the first marsupial genome sequenced was that of Monodelphis domestica, a South American species. The knowledge about mammalian genome evolution and function that resulted from studies on M. domestica is in sharp contrast with the lack of genetic data on most American marsupial species. Here, we present an overview of the chromosome studies performed in marsupials with emphasis on the South American species.

Cone visual pigments in two species of South American marsupials

Marsupials are largely confined to Australasia and to Central and South America. The visual pigments that underlie the photosensitivity of the retina have been examined in a number of species from the former group where evidence for trichromatic colour vision has been found, but none from the latter. In this paper, we report the cone opsin sequences from two nocturnal South American marsupial species, the gray short-tailed opossum, Monodelphis domestica, and the big-eared opossum, Didelphis aurita. Both are members of the Order Didelphimorphia (American opossums). For both species, only two classes of cone opsin were found, an SWS1 and an LWS sequence, and in vitro expression showed that the peak sensitivity of the SWS1 pigment is in the UV. Analysis of the Monodelphis genome confirms the absence of other classes of cone visual pigment genes. The SWS1 and LWS genes with 4 and 5 introns respectively, show the same exon–intron structure as found for these genes in all other vertebrates. The SWS1 gene shows a conserved synteny with flanking genes. The LWS gene is X-linked, as in all therian mammals so far examined, with a locus control region 1.54 kb upstream.

Physical map of two tammar wallaby chromosomes: A strategy for mapping in non-model mammals

Marsupials are especially valuable for comparative genomic studies of mammals. Two distantly related model marsupials have been sequenced: the South American opossum (Monodelphis domestica) and the tammar wallaby (Macropus eugenii), which last shared a common ancestor about 70 Mya. The six-fold opossum genome sequence has been assembled and assigned to chromosomes with the help of a cytogenetic map. A good cytogenetic map will be even more essential for assembly and anchoring of the two-fold wallaby genome. As a start to generating a physical map of gene locations on wallaby chromosomes, we focused on two chromosomes sharing homology with the human X, wallaby chromosomes X and 5. We devised an efficient strategy for mapping large conserved synteny blocks in non-model mammals, and applied this to generate dense maps of the X and 'neo-X' regions and to determine the arrangement of large conserved synteny blocks on chromosome 5. Comparisons between the wallaby and opossum chromosome maps revealed many rearrangements, highlighting the need for comparative gene mapping between South American and Australian marsupials. Frequent rearrangement of the X, along with the absence of a marsupial XIST gene, suggests that inactivation of the marsupial X chromosome does not depend on a whole-chromosome repression by a control locus.

Identification of novel major histocompatibility complex class I sequences in a marsupial, the brushtail possum (Trichosurus vulpecula)

The major histocompatibility complex (MHC) is an essential part of the vertebrate immune response. MHC genes may be classified as classical, non-classical or non-functional pseudogenes. We have investigated the diversity of class I MHC genes in the brushtail possum, a marsupial native to Australia and an introduced pest in New Zealand. The MHC of marsupials is poorly characterised compared to eutherian mammal species. Comparisons between marsupials and eutherians may enhance understanding of the evolution and functions of this important genetic region. We found a high level of diversity in possum class I MHC genes. Twenty novel sequences were identified using polymerase chain reaction (PCR) primers designed from existing marsupial class I MHC genes. Eleven of these sequences shared a high level of homology with the only previously identified possum MHC class I gene TrvuUB and appear to be alleles at a single locus. Another seven sequences are also similar to TrvuUB but have frame-shift mutations or stop codons early in their sequence, suggesting they are non-functional alleles of a pseudogene locus. The remaining sequences are highly divergent from other possum sequences and clusters with American marsupials in phylogenetic analysis, indicating they may have changed little since the separation of Australian and American marsupials.

For Mammals, Loss of Yolk and Gain of Milk Went Hand in Hand

For Mammals, Loss of Yolk and Gain of Milk Went Hand in Hand