Introduction
brief ancestral tree
main trees
monotremes
metatherians
eutherian mammals
- atlantogenata (105mya)
- boreoeutheria

evolution of mammals

Introduction

mammals evolved 201-227 million years ago and are group under the synapsids which evolved separately to the reptiles and dinosaurs (and thus separate to birds) but from a common basal amniote ancestor
basal amniotes evolved from tetrapod amphibian ancestors around 315mya and are characterized by having eggs fertilized within the mother or laid on ground
mammals are characterized by:
- the females having breasts which produce milk
- brain has a neocortex
- middle ear has 3 bones
- mammalian TMJ
  - the mammalian TMJ replaced the primary jaw joint between the articular and quadrate, found in all non-mammalian vertebrates, with these bones adapting to new roles in the mammalian middle ear
  - the evolution of the mammalian TMJ is closely related to changes in the dentition and food processing that occurred early in synapsid (mammal lineage) evolution
  - mammals have teeth that differ from those of most other jawed vertebrates. These differences include a single replacement, rather than continual loss and replacement of teeth (diphydonty rather than polyphydonty), heterodonty (varied tooth shapes in different parts of the jaw) rather than homodonty (uniform tooth shapes throughout the jaw), and most importantly for the evolution of the TMJ, occlusion of the upper and lower dentition.¹⁾
- skin has fur or hair
- having megakaryocytes without normal cell division (probably due to an epigenetic change in a single animal 220mya which then was reinforced by natural selection) which produce blood clotting fragments - platelets without nuclei (reptiles and birds have blood clotting cells with nuclei)
  - this epigenetic change then ultimately led to the development of the placenta over a period of 120 million years - the ability to clot wounds is an essential element of live birth by means of a placenta, since the placenta splits from the mother’s uterus during the birth process
- having only 16 nicotinic acetylcholine receptors (nAChR) instead of 19 as in ancestral vertebrates ²⁾
- PACAP precursor (and the new PRP gene) is now on a different gene to the GHRH precursor gene (and the new C-peptide gene) whereas in non-mammals GHRH-like peptide and PACAP are located on the same precursor ³⁾
- Placental development and genomic imprinting co-evolved with parental conflict over resource distribution to mammalian offspring (monotremes do not have genomic imprinting of IGF-2 gene but other mammals do)
- protein ZNF274 found in mammals but absent in older reptiles, fish, etc regulates the moment at which specific chunks of the genome are duplicated prior to mitosis, a process linked to epigenome maintenance, 3D organization and nucleus organization
- pivotal role of LINE-1 elements in pre-implantation development and totipotency ⁴⁾
  - mammalian genomes contain hundreds of thousands L1s that have accumulated since the origin of mammals and unlike non-mammalian vertebrates, a single group of very similar elements is active at a time in mammals, thus a single lineage of active families has evolved in this group whereas in non-mammalian vertebrates there is a large diversity of concurrently transposing families, which are all represented by a very small number of recently inserted copies ⁵⁾
  - LINE-1, a type of retrotransposon, is actively transcribed in the earliest stages of development, marking its presence as soon as the zygote forms.
  - its dynamic expression correlates with zygotic genome activation (ZGA), a key process in which the embryo transitions from relying on maternal RNA to independently initiating its gene expression.
  - activation of LINE-1 facilitates the opening of chromatin architecture, allowing essential transcriptional programs to be established
  - LINE-1 interacts with epigenetic regulators, including DNA methylation, histone modifications, and RNA methylation, ensuring precise control of gene expression
  - LINE-1 also plays a key role in stem cell biology, influencing embryonic stem cells (ESCs) and induced pluripotent stem cells (iPSCs)
  - regulation of LINE-1 has further implications in aging and age-related diseases
endothermy - a key characteristic of mammals that is shared with birds is warm-bloodedness or endothermy which allowed them to be active day and night
- endothermy was likely the starting point where mammalness evolved:
  - the acquisition of an insulating fur coat (probably via mutation of MSX2 occurred at the evolutionary root of the Probainognathia some 245 million years ago); the evolution of a larger brain, supplied with warmer blood; a faster reproduction rate; and a more active life are all defining mammalian traits that evolved because of warm-bloodedness.
  - endothermy appears to have appeared in mammalian ancestors some 33 million years prior to the origin of mammals, and endothermy evolved very quickly in geological terms, in less than a million years according to studies of the semicircular canal geometry:⁶⁾
  - The viscosity of endolymph in the semi-circular canals is critical to the balance organ’s ability to efficiently detect head rotation and aid balance. The endolymph’s viscosity would normally be altered by the evolution of a higher body temperature - in mammals, the canals adapt to higher body temperature by changing their geometry.
  - the earliest mammals were nocturnal and couldn’t rely on their eyes to feel their environment. So, together with hearing and smell, the presence of tactile hairs on the face and body of our nocturnal ancestors played an important role in their survival and stimulated the development of the neocortex. The development of the brain, an expensive organ that needs a lot of energy and produces a lot of heat, in turn played a role in the evolution of endothermy.⁷⁾
mammalian mucins mainly evolved via protein DNA gaining repeated sequences ('PTS repeats') with a high content of the amino acids proline, threonine and serine which converts it from a non-mucin protein to a mucin protein⁸⁾
primarily nocturnal
- placental mammals were mainly or even exclusively nocturnal through most of their evolutionary story, starting with their origin 225 million years ago, and only ending with the demise of the non-avian dinosaurs 66 million years ago, and most mammals are still nocturnal.
- evolved features to support nocturnal life and survival:
  - small size to enable evading dinosaurs and hiding in the undergrowth
  - lost two of the 4 retinal cones reducing color vision from tetrachromatic to dichromatic (apes later developed trichromatic to give a survival advantage in detecting ripe fruit and fresh green leaves)
  - acute sense of hearing, including coiling cochleae, external pinnae and auditory ossicles.
  - very good sense of smell, well developed nasal turbinates. Most have a large olfactory bulb.
  - well-developed sense of touch, particularly the whiskers
  - with the exception of higher primates, very large cornea, giving a less acute visual image compared to birds and reptiles.
  - endothermia that enabled early mammals to become independent of solar radiation and environmental factors
  - unique type of brown adipose tissue, allowing mammals to generate heat quickly.
  - mitochondria with respiration rates five to seven times higher than those of reptiles of similar size.
  - fur to assist in thermo-regulation in a cold (night) environment
  - lack of an ocular shielding mechanism against (diurnal) ultraviolet light.
  - loss of the ability to produce gadusol, a chemical which protects against the sun
  - the photolyase DNA mechanism, which relies on visible light, does not work in the placental mammals, despite being present and functional in bacteria, fungi, and most other animals
  - circadian rhythm and behaviour patterns in all basal groups are nocturnal, at least in placentals
  - burrowing lifestyle allowing sheltering from climate and diurnal predators appears to be a basal mammalian trait.

brief ancestral tree

primordial RNA cell
- bacteria
  - bacterial precursor of mitochondria
    - eukaryocytes evolve from endosymbiosis of procaryocytes with mitochondrial DNA creating complex cells oxidative mitochondrial capacity as well as anaerobic pathways (1,450 mya)
      - multi-celled organisms
        
        Choanozoa (950mya)
        
        Animals (760mya) - nearly all animals have a dramatically shrunken mitochondrial gene count of only 13 protein coding genes the other thousands have been relocated into the host nucleus DNA
        
        Eumetazoa
        
        Parahoxozoa (680mya)
        
        Bilateria (bilaterally symmetric body plan arose c650mya)
        
        Nephrozoa (650mya; excretory organs and nerve cords - eg. early marine worms)
        
        Protostomia (610mya) (the first opening (the blastopore) becomes the mouth)
        
        Deuterostomia (the first opening (the blastopore) becomes the anus)
        
        Chordata (notochord, a dorsal nerve cord, pharyngeal slits, an endostyle, a post-anal tail)
        
        two basal vertebrate tetraploidization events 1R/2R duplicating the genome
        
        Vertebrata (525mya)
        
        jawed fish / gnathostomes
        
        lobed fish
        
        amphibia (c370mya)
        
        tetrapod amphibia (c367mya) Devonian mass extinction 360mya
        
        Reptiliomorpha
        
        basal amniotes (c312mya eggs fertilized within the mother or laid on ground)
        
        synapsids (earliest known is 318mya)
        
        mammals (201-227mya)
        
        prototheria (monotremes)
        
        metatheria (marsupials)
        
        eutherian mammals
synapsids (earliest known is 318mya) the largest terrestrial vertebrates in the Permian period, 299-251mya
- characterized by having differentiated teeth (canines, molars, incisors);
- Eupelycosauria
  - Sphenacodontia
    - Therapsida - egg-laying (oviparous)
      - Anomodontia
        
        Chainosauria
        
        Dicynodont (270-201mya) survived Permian extinction; 70 genera of herbivores with tusks - the most abundant and diverse vertebrates on land just before dinosaur times but became extinct in late Triassic
        
        Lystrosaurus is a herbivorous (plant-eating) egg-laying Dicynodont therapsid ⁹⁾ famous for surviving the “Great Dying”, which was a major mass extinction of species 252 million years ago.
      - Neotherapsida
        
        Theriodontia
        
        Eutheriodontia
        
        Therocephalia - survived Permian extinction but became extinct in the Triassic
        
        Cynodontia - survived Permian extinction
        
        Probainognathia
        
        mammals (201-227mya)
        
        prototheria (monotremes)
        
        metatheria (marsupials)
        
        eutherian mammals

main trees

prototheria
- monotremes probably evolved around 220mya - perhaps they were the 1st mammals? (oldest fossil is 123mya)
  - egg laying mammals with bird-like ZW sex chromosomes (although echidna only has 4 Y chromosomes) and reptilian features including venomous spurs, and reptilian gait
- eutherian sex chromosomes lie on autosomal chromosome 6, while sex determination appears to be more like birds
mammals with 2 pairs of XY sex chromosomes, a new SRY gene, a placenta, nipples, and give birth
- mammals replace baby teeth with adult teeth only once unlike most other vertebrates
  - mammal teeth are attached to the jaw by gomphosis which is a ligament attachment whereas other vertebrate teeth are attached to the jaw by ankylosis, which is a hard-tissue fusion of bone to tooth
  - mammal's reduced rates of tooth replacement and a flexible ligament attaching the tooth to the jaw are needed for true tusks to evolve
- theria c166mya
  - not egg laying; lost the coracoid bone
  - mammalian placentae are unique and characterized by trophoblast syncytialization (syncytial trophoblast), where adjacent cells fuse to produce cells with more than a single nucleus, which is accompanied by expression of an endogenous, retrovirus-derived syncytin protein
  - metatherians and eutherians probably diverged 148mya ¹⁰⁾
  - metatherians c125mya in Asia
    - give birth to relatively undeveloped young
    - marsupials (?100mya in Utah) 65mya (young are carried in a pouch)
      - in common with reptiles and monotremes, marsupials lack a corpus callosum and have a lower body temperature than therian mammals (marsupials are only 35degC, monotremes are 31degC)
      - unlike eutherians, they lack homologous regions in X and Y chromosomes
      - although the genes on the marsupial X are all homologous with genes on the human X, about a third of the X genes in eutherians are autosomal in marsupials
      - The Y chromosome of marsupials is very tiny because it is derived from the smaller X of ancient mammals which did not include the added region which eutherian X have, but it retains several genes, some shared with the human Y, others unique to marsupials
      - in those with karyotypes X0 and XXY, the formation of testes is determined by the Y-dominant mechanism, whereas the other traits characteristic of males and females depend on the X-chromosome dose
      - formation of a pouch in female or a scrotum in male depends on the X-chromosome dose
  - eutherian mammals c161mya?
    - amniotic sac surrounds the fetus, lack epipubic bones
    - have a corpus callosum and body temperature is higher at 37degC
    - presence of homologous regions in X and Y chromosomes - the so-called (“pseudoautosomal region”)(Burgoyne, 1982), in which conjugation and recombination take place during meiosis
    - the X is completely conserved in mammals with same order of genes in humans as with other eutherians
    - SRY on the Y chromosome is the mammalian sex determining gene, and drives the usual autosomal sex determination mechanisms in non-mammalian vertebrates (SOX9 - is highly conserved and is pivotal in sex determination in all vertebrates)¹¹⁾
    - three ancestral blocks (different autosomal regions) that merged with the marsupial X / ancient X during the formation of the eutherian sex X chromosome have been described:
      - those arranged in the same order that in the chicken chromosome 1
      - genes in the ancient conserved region of the human X chromosome correspond to the genes in chromosome 4p of the chicken and microchromosomes of other birds as well as to the short arm of chromosome 8 of marine turtles
      - genes near ZFX on the short arm of the human X map, not to the X, but to chromosome 5 in kangaroos and chromosome 3 on the dunnart

monotremes

monotremes probably evolved around 220mya (oldest fossil is 123mya) and are egg laying mammals sharing some genes with birds (the vitellogenin genes, and they have 5 pairs of sex chromosomes and that one of the X chromosomes resembles the Z chromosome of birds, suggesting that the two sex chromosomes of marsupial and placental mammals evolved after the split from the monotreme lineage)
structural differences in their brains, jaws, digestive tract, reproductive tract, and other body parts compared to the more common mammalian types
- in common with reptiles, they have a single duct (the cloaca) for their urinary, defecatory, and reproductive systems - only semen passes through the penis which is similar to the turtle; urine is excreted through the cloaca
- lactation is via skin openings as they do not have nipples and their milk contains a highly expressed antibacterial protein not found in other mammals
- in common with reptiles and marsupials, monotremes lack a corpus callosum - L&R hemisphere communication is via the anterior commissure which carries all the commissural fibers arising from the neocortex
- have extra bones in the shoulder girdle, including an interclavicle and coracoid, which are not found in other mammals
- retain a reptile-like gait, with legs on the sides of, rather than underneath, their bodies
- the monotreme leg bears a spur in the ankle region; the spur is not functional in echidnas, but contains a powerful venom in the male platypus (many non-monotreme archaic mammal groups also possess venomous spurs)
- remarkably low metabolic rate by mammalian standards with body temperature only 31degC although this may be a later adaptation to harsh environments
- extant monotremes lack teeth as adults
ancestral venomous monotreme
- platypus (17-89mya)
- echidna (17-89mya)

metatherians

evolved c125mya in Asia (give birth to relatively undeveloped young)
probably evolved from mammals
marsupials (?100mya in Utah) 65mya (young are carried in a pouch)
- Laurasian possums ⇒ North America ⇒ South America (connected to Nth America until 65mya)
  - Ameridelphia (American marsupials - oppossums)
  - Australidelphia (arose in Sth America, there is one species in Sth America, then migrated across a temperate Antarctica to Australia c55mya)
    - Australian megafauna (now mostly extinct)
    - Diprotodontia earliest fossil is 23-28mya but probably evolved long before this - up to 55mya
      - Vombatiformes
        
        30-40mya: koalas evolve from wombat-like ancestor
        
        25-40mya: wombats evolve
        
        Mukupirna (25mya); koala, wombats, marsupial lions, marsupial tapirs,
        
        giant wombats - largest known wombat, Phascolonus at 360kg went extinct 40,000yrs ago
      - Phalangeriformes
        
        possums
      - Macropodiformes
        
        20mya, 1st hopping kangaroos evolved
        
        15mya: Ganguroo robustiter, a possible ancestor of modern kangaroos
        
        potoroos, kangaroos, wallabies
    - Peramelemorphia omnivorous bandicoots and bilbies
    - Notoryctemorphia marsupial moles
      - 20mya early marsupial moles
    - Dasyuromorphia
      - most of the Australian carnivorous marsupials
      - quolls, dunnarts, the numbat, the Tasmanian devil, and the extinct thylacine

eutherian mammals

evolved around 161mya
characterized by having an amniotic sac which surrounds the fetus and a lack epipubic bones
from 55mya to 34mya, Western Europe and Eastern Asia formed two distinct land masses with very different mammalian faunas:
- European forests were home to endemic fauna such as Palaeotheres (an extinct group distantly related to present-day horses, but more like today’s tapirs)
- Asia was populated by a more diverse fauna including the mammal families found today on both continents
34mya, Western Europe was colonised by Asian species, leading to a major renewal of vertebrate fauna and the extinction of its endemic mammals, a sudden event called the ‘Grande Coupure’ perhaps via traversing “Balkanatolia”, a forgotten continent which today covers the present-day Balkans and Anatolia

atlantogenata (105mya)

originated and radiated in the South American and African continents
afrotheria: aardvarks, elephants, sea cows, dugongs
xenarthra: anteaters, armadillos in the Americas 59mya

boreoeutheria

“northern beasts” evolved 80-100mya most males have external testes;
Laurasiatheria evolved 99mya on the continent of Laurasia
- Eulipotyphla (hedgehogs, shrews, moles)
- Scrotifera (males have a scrotum)
  - Chiroptera: bats and flying foxes
  - Ferungulata
    - Ungulates
      - Militocodon lydae 65mya rat sized mammal was probably the ancestor of all ungulates ¹²⁾
      - Cetartiodactyla (even-toed ungulates)
        
        suinea (pigs, hippopotamus)
        
        Cetacea (45-53mya): 4 legged aquatic whale-like species
        
        Perucetus colossus 37mya heaviest whale ever at 300 tonnes although at 60' not as long as blue whales which reach 100' long at 200 tonnes
        
        toothed whales (40mya - mass extinction toothed baleen whales 23mya¹³⁾)
        
        dolphins, porpoises
        
        baleen whales (25mya)
        
        Selenodont (camels, giraffe, deer, antelope, cattle)
        
        Giraffoidea (giraffes)
        
        cervoidea (deer)
        
        caprinae
        
        sheep
        
        goats
        
        ibex
        
        bovinae
        
        antelopes (16-18mya)
        
        African buffalo
        
        Bubalina genus (13,7mya)
        
        water buffalo (India)
        
        Bovina genus (13.7mya)
        
        steppe bison Bison priscus (2-5mya)
        
        European bison (wisent) theoretically the result of hybridization between Bison priscus and the ancestors of the aurochs (Bos primigenius) which apart from the lowland European bison, became extinct in 1927
        
        yak
        
        cross to America via Bering land bridge 1-0.22mya to evolve into:
        
        Bison latifrons (giant bison or longhorn bison) 0.5mya but became extinct during the Quaternary extinction event 21,000-30,000yrs ago
        
        Bison antiquus 0.25mya
        
        B. occidentalis the modern American bison 5,000-10,000yrs ago
        
        Eurasian auroch (2mya in India then migrated to the Near East 270,000yrs ago and to Africa c25,000yrs ago; by the 13thC, their range was reduced to around the Poland region where they became extinct in 1627, but were the ancestor of all domesticated cattle and possibly, the European bison)
        
        human domestication in southern Asia results in the drought-tolerant South Asian subspecies of zebu cattle Bos indicus c8,000-10,000 yrs ago
        
        human domestication in the Near East leads to the Eurasian taurine subpecies c8,000-10,000 yrs ago
        
        (presumably) humans cross Bos taurus cattle of European origin with zebu cattle to form modern Middle Eastern cattle herds 4,000yrs ago
        
        Perissodactyla: odd-toed ungulates, including horses, donkeys, zebras, rhinoceros
        
        humans first domesticated donkeys (E. africanus) c5000BC in NE Africa
        
        the oldest human-bred hybrid animal was the sterile kunga in Sumerian Mesopotamia c3200BC, a donkey cross-bred with a male Syrian wild arse (E. hemionus), the kunga hybrid was up to 6x more valuable than a donkey as they were stronger for towing vehicles, whereas the arse could not be domesticated
        
        the mule, is the sterile offspring of male donkeys and female horses (the offspring of female donkeys and male horses are called hinnies)
        
        Syrian wild arse went extinct in 1929
        
        humans first domesticated horses in east Asia
    - Ferae:
      - Hyaenodontidae (c66mya extinct) the 1st mammalian carnivores in Africa and lacked post-carnassial crushing molar teeth which limited foods to meat - the 22mya Simbakubwa kutokaafrika was a hyena-like apex predator in Africa larger than a polar bear
      - Oxyaenids (c55mya now extinct) - specialized climbing carnivores with teeth designed for crushing and preyed on other terrestrial vertebrates, eggs and insects, and may be related to pangolins
      - Pholidota (pangolins)
      - Carnivora (42-50mya; evolved in Eurasia and moved south to Africa; cats, hyenas, dogs, bears, seals)
        
        caniforms
        
        Arctoidea evolved c46mya
        
        Ursoidea
        
        Ursidea (bears)
        
        Hemicyonidae (extinct dog-bears)
        
        Pinnipedia (seals)
        
        Musteloidea (pandas, weasels, skunks, raccoons)
        
        Leptocyon a fox-like genus 34mya
        
        Canidae
        
        Vulpini (foxes) 11.9mya
        
        Canini (11.9mya) wolf-like canids and the South American canids
        
        Cerdocyonina
        
        wolves and some “foxes”
        
        dire wolf (separate ancestor to grey wolf perhaps ~6mya; extinct 13,000yrs ago)
        
        Canina (?1mya)
        
        jackal
        
        wild dogs and wolves
        
        grey wolf
        
        new world wolves
        
        Mexico
        
        North America/Hokkaido
        
        old world wolves
        
        Middle East wolves
        
        Eurasian wolf / dog common ancestor (36,000yrs ago) - these would have had a relationship with hunter-gatherers of the time who are likely to have influenced the evolution of dogs by selection of those more amenable to working with humans and resultant higher rates of mutual survival
        
        European wolves
        
        Asian wolves
        
        domestic dog ancestors (domestication started over 15,000yrs ago with Asian and European lineages)
        
        1st European dogs c15,000yrs ago
        
        1st far eastern Russian dogs c12,000yrs ago
        
        dingo / New Guinea singing dog (evolved in Asia partly from the Tibet wolf and earliest Australian fossils date to around 3,300yrs ago)
        
        domestic dog ¹⁴⁾
        
        feliformia
        
        Felidae
        
        Panthera big cats (6.37mya) eg. Panthera blytheae 4.1−5.95mya in Tibet
        
        snow leopard and tiger ancestor (3.9mya)
        
        tiger (3.2mya)
        
        jaguar (3.6mya)
        
        lion (2mya)
        
        leopard (2mya)
        
        Felinae smaller cats, can't roar but can purr as vocal folds shorter than 6mm and have restractile claws and diverged from Pantherinae around 11.5mya
        
        Leptailurus - serval
        
        Leopardus - spotted American small cats eg. ocelot
        
        Lynx
        
        Acinonyx (cheetah)
        
        Puma
        
        Felis - wildcats and domesticated cats
euarchontoglires supraprimates 85-95mya
- glires (rabbits, rodents)
- euarchonta “true ancestors” (excludes rabbits, rodents) 88mya
  - Scandentia or treeshrews 86mya
  - Plesiadapiformes (extinct)
  - primatomorpha 86mya
    - Dermoptera or colugos 80mya
    - primates - 80mya
      - Strepsirrhini
      - haplorhines (dry nosed) - 63mya
        
        anthropoidea - 58mya
        
        catarrhini (Old World Monkeys) - 40 mya
        
        see also Evolution of Humans