Human Evolution Bio263 Genes and Genomes

Who is our closest relative?

Professor Mark Pallen

Human EvolutionGenes and Genomes

• Lecture 1: Who is our closest relativeAn overview of human evolution and

palaeoanthropology. Taxonomy and humanity’s place in nature. Who is our closest living relative? Evidence from morphology and molecules.

• Lecture 2: Becoming humanWhat have comparisons between human and ape

genomes taught us about what it means to be human?

Anatomically Anatomically modern modern humanshumans

Homo neanderthalensi

s

Ancient DNAMorphology

Fossil RecordMorphology

Molecular phylogenetic & genomic studies Morphology

Extinct hominins

Living primates

Population genetics studieswith mtDNA, Y-chromosome & autosomal genes

Homo sapiens

Human Evolutionsources of data

Evolutionary history versus evolutionary biologyHow is Homo sapiens

related to other species?

When did we split from our closest relatives?

When and where did our species originate?

How did humans people the world?

Was there any gene flow between our ancestors and other archaic human species?

What were the genetic changes that made us “human”?

What evolutionary processes were at work in our genomes?

What adaptive changes have occurred since we became “anatomically modern humans”?

Where did we originate and who are our closest relatives?

Charles Darwin: Origin of Species 1859• “Light will be thrown on the origin of

man and his history” Charles Darwin: Descent of Man 1871

• speculated that humans originated in Africa

• “In each great region of the world the living mammals are closely related to the extinct species of the same region. It is, therefore, probable that Africa was formerly inhabited by extinct apes closely allied to the gorilla and chimpanzee; and as these two species are now man's nearest allies, it is somewhat more probable that our early progenitors lived on the African continent than elsewhere.”

Where did we originate and who are our closest relatives?

Evidence as to Man's Place in Nature Huxley 1863 Thomas H. Huxley concluded that “it is quite certain that the

Ape which most nearly approaches man, in the totality of his organization, is either the chimpanzee or the gorilla”.

What people used to think in the 1960s

Zallinger The March of ProgressPliopithecus - Proconsul - Dryopithecus - Oreopithecus – Ramapithecus - Australopithecus africanus - Australopithecus robustus - Australopithecus boisei - Homo habilis - Homo erectus - Early Homo sapiens - Neanderthal Man - Cro-Magnon Man - Modern Man

Human lineage thought to have diverged from African apes 15-28 Ma

A misreading of Darwin…

But who is our closest relative among living primates?

Chimps and gorillas were assumed to be sister taxa

Shared traits: knuckle walking, thin enamel

Humans have Bipedalism, S-shaped

spine, bowl-like pelvisGiant brains, chins,

small snoutHairless: “the naked

ape”Tools, culture,

languageOnly doubt was did

humans branch off before or after orangs?

But no chimp or gorilla fossils

g c h

Insights from immunologyNuttall 1904, anti-human antiserum reacted

more strongly with chimp and gorilla serum than with orang or gibbon

Goodman, early 1960shuman and great ape albumins hard to

distinguish immunologically“Hominoid slowdown”, when compared to bovines

Confirmed human, chimp, gorilla relationship to the exclusion of orangsBut human-African ape distance same as chimp-gorilla

Similar results with serum protein electrophoresis

The Cladistics Revolution

birdscrocodilianstortoises turtles

lizardssnakes tuataramammals

amphibians

archosaurs

diapsids

amniotes

sauropsids

tetrapods

Amniotes are a monophyletic group

Reptiles are a paraphyletic group

Warm-blooded animals are a polyphyletic group

All taxa to be monophyletic

A taxonomic adjustment

Vincent M. Sarichand Allan C. Wilson

"Immunological time scale for hominid evolution"

Science 158, 1967, p. 1200-1203.

"that if, man and Old World monkeys shared a common ancestor 30 million years ago, then man and apes shared a common ancestor no more than 5 million years ago”

this challenge to paleontological opinion purely on the basis of biochemistry of living species was initially either ridiculed or ignored.

A recent split!

Kimura and the neutral theory1968, Motoo KimuraNeutral mutations

predominate in evolutionDownplays the role of

natural selection in DNA and protein evolution

Neutral changes should show clock-like behaviour

DNA sequence data…

Make a treePolymorphic sites

Sequence-based phylogenies

Early molecular phylogeneticsDuring 1970s and 1980s several studies

support existence of human-chimp-gorilla cladeFibrinopeptidesMyoglobinHaemoglobinsCarbonic anhydrases

But sequences all very similar—only one amino-acid change supported human-chimp clade

The trichotomy

g c h

King and Wilson (1975) found high melting temperature for human-

chimp duplex, consistent with 99% sequence identity

Sibley & Ahlquist 1984Chimp-human duplex more stable than

gorilla-chimp or human-gorilla

Resolving the trichotomy: DNA-DNA hybridisation

Contradictory results with single-gene phylogeniesBUT phylogenetic analysis of concatenated

sequences or meta-analysis of multiple phylogenies provide solid support for human-chimp clade

Resolving the trichotomy: DNA sequence data

Ruvolo 1997

Some gene sequences incongruent, as a result of lineage sorting and because two successive splits very close in time

Resolving the trichotomy: DNA sequence data

Resolving the trichotomy: DNA sequence data

Resolving the trichotomy: Morphology

Resolving the trichotomy: Morphology

Our cousins resolved

g c h

Our cousins resolved

Another taxonomic adjustment

Sub-tribe Hominina or “hominins” reserved for species on human lineage after divergence from chimps

But when and how…?

Estimates of divergence time depend on models of genetic change (rate constant or variable) and on calibration points

Human/chimp divergence corrected for the difference in the mutation rate

varies considerably across the genome.

HumanChimp

τ-speciation

τ-gene divergence

X-chromosome shows significantly lower

divergence, compared to the rest of the genome.

This may tell us something about the human/chimpanzee

speciation(Patterson et al 2006 Nature)

But when and how…?

(Patterson et al 2006 Nature)

The observed variation in human/chimpanzee

divergence can be explained by a

secondary hybridisation of the two species after

the initial speciation event

Human/chimp speciation

The myth of 98.3%Goodman argues that as

chimps and humans share >98.3% of their non-coding DNA and ~99.5% of protein-coding sequences, chimps and bonobos should join us in genus Homo.

Jared Diamond argues that humans represent a third species of chimpanzee

Field observations of chimps and bonobos undermine human uniqueness in tool use, tool creation, sexuality etc.

http://www.greatapeproject.org

“As most people know, chimpanzees share about 98% of our DNA, but bananas share about 50%, and we are not 98% chimp or 50% banana, we are entirely human and unique in that respect. It is simply a mistake to use an entirely human construct, which is rights, and apply it to an animal, which is not human. Rights come with responsibility and I have never seen a chimp fined for stealing a plate of bananas”

Steve Jones

We are not 98% chimp!

We are not 6 million years from a chimp!

6 million years

We are not 6 million years from a chimp!

but 12 million years!

http://www.sciencemag.org/ardipithecus/

Study of Ardipithecus ramidus (4.4Ma) suggest the last human-chimp ancestor was probably more human-like than chimp-like.

“Ar. ramidus lacks any characters typical of suspension, vertical climbing, or knuckle-walking. Ar. ramidus indicates that despite the genetic similarities of living humans and chimpanzees, the ancestor we last shared probably differed substantially from any extant African ape. Hominids and extant African apes have each become highly specialized through very different evolutionary pathways.”

LCA

Human EvolutionGenes and Genomes

• Lecture 1: Molecules and MorphologyAn overview of human evolution and

palaeoanthropology. Taxonomy and humanity’s place in nature. Who is our closest living relative? Evidence from morphology and molecules.

• Lecture 2: Becoming humanWhat have comparisons between human and ape

genomes taught us about what it means to be human?