Modern Primates

Primates (extant “Euprimates”)

Strepsirrhini

Lemuriformes - lemurs

Lorisiformes - lorises and galagos

Haplorrhini

Tarsiiformes - tarsiers

Anthropoidea or Simiiformes - monkeys and apes

Platyrrhini - New World monkeys and marmosets

Catarrhini - Old World monkeys and apes

Cercopithecoidea - Old World monkeys

Hominoidea - humans and apes

Hylobatidae - gibbons, siamangs

Hominidae

Ponginae - Orangutan

Homininae - Human, Chimps, Gorillas

Primates

Strepsirhini “pro-simians”

Haplorhini

Platyrrhini New World monkeys and marmosets

Catarrhini Old World monkeys and apes

Family Hominidae “great apes”

Lorisiformes Tarsiiformes

Lemuriformes

“simians” or

“anthropoids”

Cercopithecoidea Old World monkeys

Hominoidea apes

Subfamily Homininae Genus Homo and extinct relatives

Family Hylobatidae “lesser apes” (gibbons)

Mammal Phylogeny based on Multispecies Coalescent analysis of 447 genes (Song et al 2012 Proc. Nat. Acad. Sci. USA)

Primate Phylogeny based on 8 Mb DNA sequence (Perelman et al. 2011 PLoS Genet)

Scandentia – Tree Shrews 20 species Southeast Asia

Dermoptera – Colugos or “Flying Lemurs” 2 species Phillipines, Southeast Asia

Phylogeny of early fossil Primates

(Bloch et al 2007 Proc Natl Acad Sci USA 104:1159-1164)

Purgatorius - earliest Paleocene Montana

earliest known possible primate

known only from isolated cheek teeth and tarsal (ankle) bones

“plesiadapiforms” – the earliest Primates

Early Paleocene to late middle Eocene (~66-38 MY)

paraphyletic to Euprimates (“true” or “crown” Primates)

a diverse collection of ~140 species in 11 families

ranging in size from mouse to house cat

many highly morphologically specialized/derived

e.g., Carpolestidae Paleocene-Eocene North America

Plesiadapis Paleocene-Eocene North America/Europe

Teihardina – Omomyidae

early Eocene China

earliest Euprimate (true primate)

evidence that early Euprimates

were arboreal, diurnal, predators

Strepsirhini Lemuriformes Lemurs Madagascar

Strepsirhini Lorisiformes

Lorises India SE Asia

Galagos or “bush babies” Africa

Adapis

Darwinius

Middle Eocene Adapidae –

stem Strepsirhines

Notharctus

Haplorhini Tarsiiformes Tarsier SE Asia

Afrotarsius and Afroasia

presumed earliest Haplorhines

late middle Eocene to Oligocene

Egypt, Lybia, Myanmar

known only from isolated cheek teeth

Victoriapithecus 20-15 MY

Catopithecus

36-31 MY

Aegyptopithecus

33-31 MY

Earliest Catarrhines

Late Eocene to Oligocene

Africa

Earliest possible Hominoids

Proconsul Miocene 25-23 MY East Africa

Earliest Hominoids

Dryopithecus

Miocene 12-9 MY Africa, Eurasia

Earliest Hominoids

Sivapithecus (Ramapithecus)

Miocene 12.2 MY India

Earliest Hominoids

Oreopithecus

Miocene 9-7 MY Italy

Phylogeny of Hominoidea

guenons gibbons orang gorilla chimps human

Hominidae Hylobatidae

Hominoidea

Homininae Ponginae

Cercopithecoidea

Possible earliest Homininae

Miocene Africa

inferred habitual bipedality

some with reduced canines

Sahelanthropus Chad 7 - 6 MY

inferred habitual bipedality

reduced canines

Orrorin – Kenya 6.0 - 5.7 MY

inferred habitual bipedality

Ardipithecus kadabba Ethiopia

5.77 - 5.54 MY

obligate bipedality

reduced canines

Ardipithecus ramidus Ethiopia

4.51 - 4.32 MY

obligate bipedality

reduced canines

Possible earliest Homininae

Miocene Africa

inferred habitual bipedality

some with reduced canines

Sahelanthropus Chad 7 - 6 MY

Orrorin – Kenya 6.0 - 5.7 MY

Ardipithecus kadabba Ethiopia

5.77 - 5.54 MY

Ardipithecus ramidus Ethiopia

4.51 - 4.32 MY

Some key hominine taxa listed in reverse order of age

Sahelanthropus tchadensis 7 - 6 MYA

Ardipithecus ramidus 4.51 - 4.32 MY

Australopithecus afarensis 3.9 - 2.9 MY

Australopithecus africanus 3.8 - 2.0 MY

Homo habilis 2.8 - 1.5 MY

Homo ergaster 1.9 - 1.4 MY

Homo erectus 1.9 MY - 70,000 yrs

Homo naledi – 335,000 – 236,000 yrs

Homo neanderthalensis 230,000 - 30,000 years

Homo floresiensis 94,000 - 13,000 yrs

Sahelanthropus tchadensis 7 - 6 MYA

Africa, bipedal?

Gorilla

Australopithecus anamensis 4.2 - 3.9 MY Kenya, Ethiopia

probably partly arboreal

Australopithecus afarensis 3.9 - 2.9 MY Ethiopia

cranial capacity 380 - 430 cc, bipedal, possibly partly arboreal

Australopithecus africanus 3.3 - 2 MY Africa

cranial capacity 420 - 500 cc, bipedal, partly arboreal

Chimpanzee

Paranthropus spp. – robust australopithecines

Africa, evolutionary off-shoot, specialized for nut-cracking

Key finding bipedalism came first

increased brain size came later

Homo habilis 2.4 - 1.5 MY Africa, possibly Asia

cranial capacity 500 - 800 cc, Oldowan tool culture

Homo ergaster (possibly African Homo erectus)

1.9 - 1.4 MY Southern Africa, possibly central Europe

possibly the first hominin to vocalize, Oldowan and Achuelean tool cultures

Homo erectus 1.8 MY - 300,000 years, Africa and Asia

Cranial capacity 750 - 1225 cc Acheulean tool culture, fire use

Homo heidelbergensis (rhodesiensis) – “archaic Homo sapiens”

900,00 - 200,000 years, Africa, Europe

Probable funerary practice, Achuelean tool culture

from left to right: Australopithecus africanus, 2.5 million years old; Homo rudolfensis,

1.9 million years old; Homo erectus, ~ 1 million years old; Homo heidelbergensis,

~350,000 years old; Homo sapiens, ~ 4,800 years old (Photo Credit: Chip Clark, Jim DiLoreto, & Don

Hurlbert, Smithsonian Institution)

Homo neanderthalensis 230,000 - 30,000 years Europe, Middle East

Cranial capacity 1350 - 1450 cc

Homo neanderthalensis multiple tool technologies

Mousterian Keilmessergruppen Levallois

Homo neanderthalensis

Homo neanderthalensis

funerary practice

cannabalism

care for the invalid

use of pigments

body ornamentation

Discoveries still being made

Homo floresiensis discovered in 2003

estimated 18,000 years, Indonesia, 1 meter tall

Discoveries still being made

“Denisovan” discovered 2010 in cave in Siberia from which

Neanderthals were already known

originally only a phalanx (finger bone), now teeth and a skull fragment of

four other individuals

Facial reconstruction from epigenetic methylation signatures of ancient

genome

Discoveries still being made

Homo naledi thousands of bones discovered in 2013 in South Africa

Introgressive Hybridization

Neanderthal

Up to 2% Neanderthal in non-Africans, highest in East Asians

presumably due to smaller populations (Sankararaman et al Nature 2014 Mar

20;507(7492):354-7)

Neanderthal alleles that affect skin and hair may have helped

modern humans to adapt to non-African environments

Multiple Neanderthal-derived alleles confer risk for disease, i.e.,

lupus, biliary cirrhosis, Crohn’s disease, optic-disk size, smoking

behavior, type 2 diabetes, suggesting that Neanderthal alleles

continue to shape human biology

Neanderthal-derived sex-linked genes are reduced 5-fold

compared to autosomal genes, suggesting strong selection for

hybrid sterility

Denisovan

4-6% Denisovan in Melanesians (Reich et al Nature Nature 468, 1053–1060 (23 December

2010)

Introgressive Hybridization

•17% of Denisovan genome is of Neanderthal origin

•3 - 5% of modern aboriginal Australian and Melanesian genomes are

Denisovan

Teixeira and Cooper 2019 DOI: 10.1073/pnas.1904824116

Introgressive Hybridization

SRGAP2 gene

duplicated in humans but not in other primates

slows the rate of synaptic maturation and increases the density of synapses in

the cerebral cortex

duplicated in the human genome three times: 3.4, 2.4 MY, and 1 million years

ago

the 2.4 MY duplication is present in 100% of all humans (approximately coeval

with first fossil occurrence of Homo and marked increases in brain size)

the 1 MY duplication is approximately coeval with first fossil occurrence of

archaic Homo sapiens (i.e, Homo heidelbergensis)

modern Homo sapiens 160,000 - present

40,000 – 30,000 yrs painting, jewelry, carving

11,000 yrs agriculture, 6,000 yrs metallurgy

Timeline of Human Dispersal

Africa

All modern human genotypes coalesce to 150-200,000 years ago

Central and Northern Asia

Mitochondrial haplogroups A, B, and G originated about 50,000 years ago, and

bearers subsequently colonized Siberia, Korea, and Japan by about 35,000 years

ago

Newly discovered teeth date modern humans in southern China 80,000 years ago (Liu et al Nature 526: 696 29 October 2015)

Americas

Paleo-Indians originated from Central Asia, crossing the Bering Land Bridge

between eastern Siberia and present-day Alaska. Humans lived throughout the

Americas by the end of the last glacial period. Dates for Paleo-Indian migration

out of Beringia range from 40,000 to around 16,500 years ago

African populations are genetically the

most diverse and earliest divergences

among modern humans (based on 1327

microsatellite and indel loci).

Tishkoff et al Science. 2009 May 22; 324(5930): 1035–1044.

Migration of modern humans into Europe

It may have taken 15-20,000 yrs for Europe to be colonized

37,500 yrs 35,000 yrs 32,500 Yrs 30,000 yrs

Rasmussen et al. Nature 506, 225-229 (2014)

Anzick-1 Clovis gene flow from Siberian Upper Palaeolithic Mal’ta into Native American

ancestors before 12,600 years BP

Relationships of Anzick-1 Clovis

Principal components analysis of individual

genotypes. (A) Global data set and (B) African

data set.

Tishkoff et al Science. 2009 May 22; 324(5930): 1035–1044.

Native Americans represent at least three waves of

migrants from Asia

Nearly all the populations from Aleut people in Alaska to the Yaghan in

Chile originated from a single migration across the Bering land bridge

Southern populations have less genetic diversity than northern,

suggesting that their ancestors travelled quickly, probably along the

West Coast, winnowing down diversity as they moved

two later migrations from Asia gave rise to Inuit people of

Greenland and Chipewyan people from west of Hudson Bay in northern

Canada

Relationships of Anzick-1 Clovis

above, SNP Polymorphisms private to a population, private to a continental

area, shared across continental areas, and shared across all continents

right, the number of

variant sites per

genome Sherry et al Nature 526 Oct 2015

Human populations are highly differentiated but also highly introgressed

Human populations are highly differentiated but also highly

introgressed

1000 Genomes Project Consortium Nature 2015 Oct 1;526(7571):68-74

86% of rare variants restricted to a single continental group

but most variants in any individual are common and shared among continents

east–west clines exist in Africa and East Asia

north–south cline exists in Europe, Europe, and Africa

Native-American admixture exists in the Americas

Mapped Structural Variants among 2,504 living humans

Deletions (biallelic) 42,279

Duplications (biallelic) 6,025

Copy number variants (CNV) 2,929

Inversions 786

Mobile element insertions (MEI) 16,631

Nuclear mitochondrial translocations(NUMT) 168

Collapsing multiple copies of CNVs and homozygous SVs onto the haploid

reference assembly, a median of 8.9Mbp of sequence are affected by SVs,

compared to 3.6Mbp for SNPs

median 18.4 Mbp of SVs per diploid genome (CNVs 11.3 Mbp, biallelic

deletions 5.6Mbp)

65% of structural variants occur at a frequency of 0.2% and are specific to

individual continental groups

nearly all structural variants with frequency >2 % are shared across

continents

Sudmant et al Nature 2015 Oct 1;526(7571):75-81

1000 Genomes Project Consortium Nature 2015 Oct 1;526(7571):68-74

Unmapped Variants among 2,504 living humans from 26 populations

single nucleotide polymorphisms (SNPs) 84.7 million

short insertions/deletions (indels) 3.6 million

structural variants 60,000

The typical human genome

99.9% of variants consist of SNPs and short indels

2,100 to 2,500 structural variants (1,000 large deletions, 160 copy-number

variants, 915 Alu insertions, 128 LINE1 insertions, 51 SVA insertions, 4

NUMTs, and 10 inversions) total ~20 million bases of sequence

differs from the reference human genome at 4.1 million to 5.0 million sites

~2,000 variants per genome associated with complex traits

24–30 variants per genome implicated in rare disease

Population Bottlenecks

There is evidence that the first human bottleneck occurred ~50,000 years ago

when founding populations emigrated from Africa

Europeans, Asians, and Americans appear to share a strong and sustained

bottleneck (Ne <1,500) between 15,000 to 20,000 years ago, while African

populations experienced a less-severe bottleneck during the same time period

(Ne >4,250) (1000 Genomes Project Consortium Nature 2015 Oct 1;526(7571):68-74)

Evidence from Y-chromosomes suggest another bottleneck occurred only in

males between 4-8,000 years ago during a period of global growth

There was a dramatic decline in genetic diversity in male lineages with the

advent of agriculture, likely the result of the accumulation of material wealth

In contrast, female genetic diversity (based on the mitochondrial chromosome)

was on the rise during this same period

This genetic structure may predispose some populations to certain types of

genetic disorders

Hereditary inequality began over 7,000 years ago in

Europe in the early Neolithic era

The Neolithic era introduced heritable property (land and livestock) into

Europe and that wealth inequality got underway when this happened

Strontium isotope analysis of >300 skeletons

indicated that men buried with stone adzes

had less variable isotope signatures than men

buried without adzes

Early Neolithic women were more likely to

have originated from other areas, indicating

a male-centered kinship system in which

females move to reside in the location of the

males when they marry

64% of European Men are Descended from

just Three Bronze Age Warlords between

3,500 to 7,300 years ago (Batini et al Nature Communications 6: 7152 (2015)

11 dynastic leaders

believed contributed

disproportionately to

the genetic legacy of

Asia

Genghis Khan 12-13th century, with

~16 million descendants

Giocangga 16th century, with ~1.5

million descendants

nine other dynastic leaders of Asia

dating from 2100 BC and 700 AD

(Balaresque et al European Journal of Human

Genetics (2015) 23, 1413–1422)

Nurhaci, grandson of Giocangga.

Are humans still evolving?

10%–20% of amino acid changes have been adaptive, i.e.,

show signatures of selection, in human evolution (Messer & Petrov

2013 Proc Natl Acad Sci 110: 8615–8620)

There have been approximately 100 strong selective sweeps

in humans in the past 100,000 years; these occurred primarily

in regulatory rather than coding regions (Enard et al Genome Res. 2014

Jun;24(6):885-95 )

The signals of positive selection are evident in all human

populations, but stronger in the “out-of-Africa” populations,

although this could be artifactual due to demographic or other

reasons

The agricultural revolution 8,500 years ago in

Eurasia witnessed the appearance of genetic

variants associated with height, lactase

persistence, fatty acid metabolism, vitamin D

levels, light skin pigmentation and blue eye color,

and immunity

Two variants appear on genes that have been

linked to higher risk of coeliac disease but that may

have been important in adapting to an early

agricultural diet (Mathieson et al Nature 30 October 2015)

Lactase Persistence in Europeans

Ancient hunter-gatherers in Europe could not digest milk 8,000

years ago

The ability to do so only came about 4,300 years ago

Skin color in Europeans

7,700 year old remains from Sweden had light skin, blonde hair,

and blue eyes

8500 year old hunter-gatherers in Spain, Luxembourg, and

Hungary had dark skin and hair but a 7,000 yr old Spaniard had

dark hair and the dark-skinned genes of an African but blue

eyes

Central and Southern Europeans acquired genes for light skin

at about 5,800 yrs ago with admixing from the Near East

Domestication of Livestock

Estimates on the age of domestication of

dogs varies from 11-16,000 years ago to

27-40,000 years ago

Cattle were domesticated from wild

aurochs in the Anatolian Fertile Crescent

around 10,500 years ago (Orlando Genome Biology

(2015) 16:225)

Horses appear to have first been

domesticated in Eurasian steppes about

4,000 years ago

12,000 yr old human dog burial in Israel

30,000 yr old auroch painting in France

Ocellated turkey

Domestication of Plants

Earliest evidence in Southwest Asia and the Middle East to about 11,050

years ago

Americas (~9,000 yrs ago) – squash, maize, beans, cassava, potatoes

East Asia – millet, rice, soy

Middle East – peas, wheat

Independent Centers of Plant Domestication

Smith PNAS 2006;103:12223-

12228

Metallurgy

Technology that facilitated agriculture, warfare, transport, cooking, and

industrialization

Native copper fashioned into knives and sickles from about 7000 BC in Anatolia

Copper ore mined from deep shafts and smelted since 4000 BC at Rudna Glava in

the Balkans and by about 3800 BC in the Sinai

peninsula

Bronze (alloy of copper and tin) first developed

in the Middle East around 2800 BC

Egyptians made weapons of native meteoric iron

from about 3000 BC

Hittites first smelted iron in Anatolia from about

1500 BC

Cast iron historically recorded in China to 513 BC

Conquerors and Imperialism – has and continues to shape human evolution through

genocide, both concentration and deprivation of resources,

migration and introgression, socialization, and cultural

phenomena (e.g., language, technology, religion, hygiene,

education) that have changed selective pressures and

paradoxically increased

civilization

Timeline of early civilizations

Throughout human evolution there has been a

proliferation of social groups, languages, and religions

from just a few ancestral forebears

In general this is manifested as social bonding within

groups and competition between groups

Bases for social identity

Language – 7,106 registered languages worldwide

Religion – roughly 4,200 religions worldwide

Political boundaries – there are currently 196 countries and

roughly 5,000 indigenous tribes worldwide

Wealth

Language – 7,106 registered languages worldwide

http://www.sil.org/

Origins of Major Languages

http://www.linguisticsociety.org/

Long-Distance Trade

Estimates as old as 150,000 yrs (Watson 2005. Ideas: A History of Thought and Invention from Fire to

Freud. New York: Harper Collins; Smith 2008. Premodern trade in World History. Taylor and Francis)

Trade in flint and obsidian in Africa from 17,000 BC, in North America from

10,000 BC

Money

Native gold nuggets have been found in archaeological context from

40,000 years ago

Earliest forms of commodity money (i.e., obsidian, grains, cattle, cowry

shells) to at least 9,000 BC

2400 BC in the kingdom of Ur in Mesopotamia, accounts were being kept

using weights of silver

Gold has been considered valuable since at least 4000 BC. In about 1500

BC in Egypt, gold became the recognized standard medium of exchange

for international trade.

Earliest coinage (bronze spade money) from about 1000 BC

in China and manufactured coins from 700-500 BC in India,

China, and Aegean Sea

Chinese spade money 1200-800 BC

Will Humans Continue to Evolve? – with the advent of medical interventions, gene editing to correct

hereditary disease, and our ability to modify our environment in

ways that remove preexisting selective pressures?

Biological evolution is the change in frequency of heritable

characteristics, i.e., genotype frequency (and epigenetic factors,

as we are now coming to realize)

In the absence of continued selection, mutation and drift are

expected to alter allele and genotype frequency and thus erode

existing adaptations – indeed, this would be evolution albeit

nonadaptive

It is also relevant that not all people have equal access to the

aforementioned benefits of society due to social, economic, and

political factors that are themselves selective agents

There are and will continue to be new technology-driven skills,

social, economic, political, and environmental (nutrition,

environmental toxins) selective pressures

Will Humans Continue to Evolve?

Based on NOAA record-keeping beginning in 1880

• The three hottest years on record have occurred in the last 10 years

• Nine of the 10 hottest years on record have occurred in the 21st century

• Thirteen of the 15 the hottest years on record have occurred in the last 15

years

• All 15 years from 2000 on have been among the top 20 warmest years on

record

• The last 358 months in a row have been warmer than the 20th-century

average

Based on fossil foraminifera

• It took 4,000 years for the world to warm about 1.25 degrees from the end

of the ice age to about 7,000 years ago. A similar level of warming occurred

from the 1920s to the 1940s (Marcott Science)

• There is no precedent for this heat spike as far back as 11,000 years

• It may have been 125,000 years since there have been temperatures

rivaling today's

NASA data; Hansen et al 2006 Global temperature change. PNAS 103: 14288-14293

Global Warming already has

- caused changes in fisheries industries by increased temperature and

acidification, resulting in changes in distribution, poisonous algal blooms,

and die-offs

- begun opening arctic ice sheets leading to increased political tension

vying for undersea mineral and petroleum resources

- increased frequency and severity of extreme climatic events (drought,

fires, flooding, storms) leading to increased spending on disaster relief

- increased coastal flooding that is making low-lying areas uninhabitable