Evolution BIOL 3300 FINAL PREP

• 1. Measuring genetic variation
• 2. Selection
• 3. Drift and on-random mating
• 4. Migration
• 5. Combined evolutionary forces

• 1. Background
• 2. Genetic variation and genetic markers
• 3. Hardy-Weinberg law
• 4. Heterozygosity in the wild

• Developed during evolutionary synthesis
• Allows quantitative predictions of evolutionary change at the population level
• Recall that Natural selection
• - Acts on individuals and affects populations
• - Acts on phenotypes and changes allele frequencies

• 1. How much genetic variation is in natural populations?
• 2. What processes cause allele frequencies to differ between populations?
• 3. How does biology (mating patterns, fecundity, migration) affect genetic variation?

• 1. Could humans evolve resistance to HIV or Ebola? How long would that take?
• 2. Does human evolution still occur in industrialized societies where we are protected from food scarcity, predators and pathogens?
• 3. Does genetic diversity of species in restored/reclaimed sites differ from natural sites?
• 4. Will polar and alpine species be able to cope with climate change? How quickly did the polar bear evolve to survive on seal blubber; could there be reverse evolution?

Type; significance

• Point mutation; creates new alleles
• Chromosomal inversion; alleles inside inversion are transmitted together as a unit
• Gene duplication; Redundant genes may acquire new functions through accumulation of additional mutations
• Genome duplication; may create new species, massive gene duplication

Per gene mutation rate: (1 in 10,000 - 1 in 10,000,000)

• 1) Classical school: a few rare mutants
• - T.H. Morgan and H.J. Muller
• - Drosophila in lab
• - Evolution "waits for" mutational variation

• 2) Balance school: much allelic variation
• - T. Dobzhansky and E.B. Ford
• - Drosophila in natural populations
• - Evolution "waits for" environmental change

• Some evidence from visible polymorphisms
• - Shell banding patterns in snails
• - Stripes on garter snakes
• - Coat colour in mice
• - human height

Need breeding studies to confirm genetic basis

• Many species difficult to rear in captivity
• Complex inheritance of many traits
• Breeding experiments not often feasible

• "Molecular phenotypes"
• Heritable and polymorphic
• Reflect allelic (DNA) variation at a locus
• Allow direct measurement of genetic differences without breeding experiments

• Genetic variation
• - Conservation biology

• Short-term processes
• - Selection, migration, hybridization, mating patterns

• Long-term processes
• - range expansion/contraction, long-term demography, speciation, phylogenetics

• 1)Protein coding locus (allozymes)
• - Mutations affect physical properties
• - Alleles are "allozymes"
• - Applications: short-term processes esp. mating systems

• 2) DNA sequences
• - Intervening regions (introns) are "neutral"
• - Mutations accumulate over time
• - Applications: phylogenetic analysis, molecular clock, DNA barcoding
• - Expressed regions (exons) are under selection
• - Changes that affect gene can be a "signature of selection"

• 3) Tandem repeats (STR = microsatellites, VNTR)
• - "Neutral regions" containing repeats of the same nucleotide sequence (e.g. TATATATATATATA)
• - Repeat number highly variable among individuals
• - Applications - paternity, forensics, population differentiation

• 4. Point mutations detected through DNA fragment analysis (e.g. RAPDs, AFLPs)
• - Restriction enzymes: cut DNA at specific sequence
• - Nucleotide changes can add or substract restriction sites
• - Numerous, variable bands within species
• - (SNP's, single nucleotide polymorphisms, detected directly through sequencing)

• Relates Mendelian segregation to to genotypic frequencies in "ideal" situation
• Works because transmission of alleles to gametes is predictable

• 2 allele case: p^2 + 2pq + q^2 = 1.0
• Useful null hypothesis

• Assumptions:
• 1. No mutation
• 2. Random mating
• 3. Infinitely large population
• 4. No migration
• 5. No selection
• 6. (Diploid organism, sexual, non-overlapping generations)

Heterozygosity (H): proportion of heterozygotes in a populations

• He = expected heterozygosity
• Ho = observed heterozygosity

When allele a freq. = 0.5, highest proportion of heterozygotes in population

• Evidence from allozymes (=isozymes)
• Mean heterozygosity (H bar): averaged over loci

Recall - maximum heterozygosity is 0.5 when 2 alleles are present

BALANCE SCHOOL SUPPORTED

Population genetic theory predicts how departures from H-W affect populations

• General approach:
• - relax assumption individually
• - relax assumptions in combination

• 1) Quantifying selection
• 2) General selection model (modifying HW)
• 3) directional selection
• 4) non-directional selection

• Until 1930's biologists assumed that selection was too weak to measure
• Discovery of (a) industrial melanism in moth & (b) heavy metal tolerance in plants changed this view

--> many studies of polymorphisms

s = 1 - w (of least fit phenotype)

Omega = fitness

• Direct measurement:
• - Compare survival or reproduction by phenotypes or genotypes
• - Ideally full life cycle
• - Often single component of life cycle

• Change in genotype frequency over lifespan:
• - compare zygotes, adults, adults that mate

• e.g. Feral pigeons in California
• - Wildtype: blue-grey with white rump recessive
• - "Other": rump colour = plumage colour

Hypothesis: White rump increases change that pigeons will avoid falcon attack compared to "blue bar" phenotype

• VIABILITY SELECTION
• Observational study 
• - Observed 1,485 attacks
• - Wild type (white rump): 90% escape attacks
• - Blue bar (blue rump): 10% escape attacks

• Experiment:
• - reverse phenotypes by gluing feather on 756 pigeons
• - Blue rumps on wild type: 10% escape attacks
• - White rumps on blue bar: 90% escape attacks

• Hypothetical clutch size:
• - Wild type (white rump): 4 chicks per year
• - Blue bar (blue rump): 8 chicks per year

• a) fitness of all phenotypes
• b) frequency of each phenotype in the population

• Genotype:      A1A1  A1A2  A2A2
• Freq. before     p²      2pq      q²
• selection
• Fitness         ω_A1A1 ω_A1A2   ω_A2A2
• Freq. after
• selection*     p² ωa1a1/ωbar etc.
• (*gives)

• ω bar/mean fitness = 
• p^2ωA1A1 + 2pqωA1A2 + q^2ωA2A2

• One allele is consistently favoured over the other(s)
• The fitness of the population is highest when the population is "fixed" for the favoured allele

• Per generation rates of change depend on...
• - fitness differences
• - proportion of each phenotype in the population

• Lethal recessive allele in flour beetles (Tribolium castaneum)
• - Recessive alleles change slowly when rare
• - Dominant alleles change slowly when common

• e.g. peppered moths
• - journal of Heredity
• - Monitored moths in Britain and Michigan as industrial particulates decreased

• Directional selection eliminates variation
• Both strong selection and high variation occur in nature

• Neutralists: Molecular (marker) variation results from mutation and drift
• Selectionists: Generic variation is maintained by non-directional selection ... and/or variation in the direction of selection

• a) Overdominance (heterozygote advantage)
• e.g. sickle cell anemia
• Heterozygote favoured in regions with malaria

b) Negative frequency dependence

c) Multiple optimal phenotypes

d) trade-offs

e) varying selection

• e.g.Colias (sulfur) butterflies
• Allozymes for PGI (phosphoglucoisomerase)
• Allele 1: low temp activity
• Allele 2: stability at high temps

Measured genotype freq. over lifespan

Fitness of each phenotype negatively related to its frequency

e.g. parasite-host interactions, rare prey advantage

• e.g. Elderflower orchid in Europe
• - orchid with no reward for pollinators
• - "generalized food mimic"
• - plant fitness highest when visited
• - insect fitness highest when avoid plant

Colour polymorphism within populations (usual in plants)

• Hypothesis
• -Rare colour morph will receive more visits

Experiment

• - Artificial populations with varying frequencies of each morph
• - Measured male fitness:
• With greater freq. of yellow morph -> decr. relative male reproductive success (pollen removed)

• - Measured female fitness:
• same trend (fruit set)

Decr. variation within populations, may maintain within species

• Underdominance - heterozygote disadvantage
• Positive frequency dependence:
• e.g. Mullerian mimicry in Heliconius butterflies

• Alleles that enhance one fitness component but decreases another may be maintained at intermediate freq.
• e.g. mating displays

Spatial or temporal variation in selection pressure is likely common

• 1. H-W equations can be modified to make quantitative predictions
• 2. Directional selection can rapidly eliminate genetic variation
• 3. There are many types of non-directional selection
• - Most maintain variation within populations
• - A few reduce variation within populations but may maintain variation within species
• 4. How strong is selection relative to other evolutionary forces?

• 1. Types of non-random mating
• 2. Inbreeding depression
• 3. Purging of deleterious alleles

• a) Negative assortative mating
• - Opposites attract
• - Maintains polymorphisms at relevant loci

• b) Positive assortative mating
• - like with like
• - Incr. homozygosity at relevant loci

Overlaps with frequency dependent selection

• c) Inbreeding - mating among relative
• - Incr. homozygosity across entire genome

• Inbreeding increasing expression of all recessive alleles
• Increases expression of deleterious alleles can reduce fitness in inbreeding populations

δ = 1 - ω_inbred/ω_outbred

• Example King Tut possibilities:
• - Parents were full sibs?
• - Two congenital defects?
• Clubfoot
• Partial cleft palate

• Married half sister?
• - two unborn children

... The end of the dynasty?

• δ is often more severe late in life
• δ may be more severe under stress

e.g. Age related increases in fruit flies. Inbreeding depression increases with age (days)

• Sustained inbreeding
• - Deleterious recessives should be "purged" from the population
• - Hope for conservation??

• 1. Definition of genetic drift
• 2a. effect on heterozygosity (H)
• 2b. Effect on population differentiation (Fst)
• 3. Drift, selection, and inbreeding

• Alleles are sampled to form zygotes during random mating
• Adult are a sample of the zygote pool
• Each generation is a sample of the previous generation

• "Random changes in allele frequency due to sampling error"
• Strongest when sample size, i.e. population size, is small
• Drift is random
• - No allele or genotype favoured

Rare alleles tend to be under-sampled

• Allele frequency in one generation affects gamete pool for the next generation, leading to two major outcomes.
• a) loss of heterozygosity and fixation for a single allele
• b) Differentiation among population

- effects are most dramatic in small populations

H_g+1 = H_g[1 - 1/2N]

Rate is inversely related to population size

• 107 populations of N = 16
• Founders all heterozygous for eye colour
• Heterozygosity decreased over generations

Also bottleneck - loss of heterozygosity e.g. cheetahs

• Fst - single locus measure of population differentiation
• Fst = var(p)/pbar(1-pbar)

• Low differentiation: Fst --> 0
• High differencetiation: Fst --> 1

Gst - multilocus equivalent

• e.g. eveningsnow flower (Linanthus dichotomus)
• Early studies of drift

• Population size = 400 
• Gen 0:
• All p = 05
• Fst = 0

• Gen 100:
• Variation in p 
• Fst > 0

• Heterozygosity may be identical between subpopulations, but allele frequencies can be still be different
• Pop 1. P = 0.1   2pq = 0.18
• Pop 2. P = 0.9   2pq = 0.18

• Drift leads to random loss of alleles, whereas selection maintains one or more alleles
• What happens when a favoured allele is at low to moderate frequency in a small population?
• Combined effects depend on population size (N), strength of selection (s), allele frequency

- Drift overrides selection when s << 1/2N

- Selection overrides drift when s >> 1/2N

May be effective when increased inbreeding is gradual and population size is not small

• ...but
• Small populations experience both drift and inbreeding
• - mildly deleterious alleles are more likely to be fixed when N is small (s << 1/2N)
• - this may increase inbreeding depression, further reduce N, and cause fixation of additional deleterious alleles

• Study of New Zealand native and introduced birds
• Measured hatching failure and analyzed as a function of past "bottleneck" = minimum population size recorded
• a. birds native to N.Z.
• (b. birds deliberately introduced to N.Z.)

Increase in hatching failure with increasing severity of population bottleneck in native New Zealand birds (n=22)

• 1. Definition and models
• 2. Effects on population differentiation
• 3. Effects on allele frequency
• 4. Benefits and drawback of migration

Migration causes gene flow, the movement of alleles from one population to another

• 2 components to gene flow
• - gene movement
• - gene establishment

The "Jekyll and Hyde" of evolution?

• Island model 
• Stepping stone model
• Isolation by distance
• Metapopulation model

• Gene flow homogenizes populations
• Fst ~= 1/(4Mn+1) when m<0.01
• N = effective population size
• m = migration rate
•     = proportion           migrants/generation

Fst at equilibrium and Nm are negatively correlated (negative exponential)

• e.g. When Nm = 1, Fst = 0.2
• 1 migrant/generation has a large effect

• Neutral genetic markers can be used to estimate Nm (number of migrants per generation)
• 1/(4Nm+1) = Fst = var(p)/pbar(1-pbar)

• P' = p_sink(1-m) + p_source(m)
• q' = q_sink(1-m) + q_source(m)

• Habitat loss in Illinois 
• Protection and habitat restoration since 1960's
• 1970's - 1990's populations in decline

• Recall Extinction vortex (mutational meltdown)
• - small populations are very susceptible to both drift and inbreeding
• Recall drift stronger when s << (1/2N)
• Deleterious alleles fixed
• --> further reduction in N, more drift, more inbreeding

• Rescue through MIGRATION
• Artificial migration (increases effective N)

• Collared lizards
• Florida panthers

• Migration may prevent or reduce local adaptation by bringing in deleterious alleles
• Equilibrium allele frequencies depend on the strength of selection relative to the rate of migration

• Lake Erie water snakes
• Banded allele from mainland detrimental on island
• Banded allele is present on island due to migration

• Within any population, reflects balance between selection and migration
• Across wide range see "isolation by distance effect"
• Neutral alleles in combination should show steady change (adjacent areas most similar)
• Selected alleles should show sharper gradients

• e.g. Lactate Dehydrogenase-B (LDH-B^b) in Fundulus heteroclitus 
• LDH-Bb has higher catalytic activity at low temperatures
• Gradient in frequency over northern latitudes (favoured/selected (not neutral) in northern latitudes)
• Very small gradient over latitudes if neutral alleles

• Homogenizes allele frequencies across populations (reduces Fst)
• - May alleviate affects of drift (and inbreeding) = "Jekyll" effect
• - May prevent adaptation to local conditions by bringing unsuitable alleles = "Hyde" effect or "migration load"

• Evoluntionary importance?
• Adaptive Landscapes
• Shifting balance theory

• Natural populations experience all evolutionary forces simultaneously
• Which processes are most important in determining evolutionary change?

• Evolutionary synthesis:
•  - Evolution results from changes in frequency of Mendelian genes

Wright & Fisher disagreed on relative importance of natural selection, drift, & migration

• Fisher/Wright
• Refining existing adaptation/Origin of adaptive novelty

Selection + mutation/ Selection + drift +gene flow

Large, panmictic populations/small,subdivided populations

Additive gene effects/epistasis and pleiotropy

• "A visual aid for non-mathematical biologists" Carneiro & Hartl 2010
• "One of the most popular [metaphors] in the history of biology" Orr 2009

• Appealing to organimal and molecular biologists
• Complex fitness landscapes are analogous to topographic maps
• "Elevation lines" represent population mean fitness for given allele frequency

• Wright
• Populations occupy a position on "adaptive landscapes"
• Changes in allele frequency correspond to changes in phenotype and changes in population mean fitness
• How do populations cross"fitness valleys?"
• Local optimum - valley - global optimum

Phase 1. Drift drives a population across a fitness valley

Phase 2. Selection drives the population to a new optimum, which is a global optimum (or at least higher than the original optimum)

Phase 3a. The population at the global optimum grows large and send out many migrants to neighboring populations

• Phase 3b. The migrants change allele frequency in recipient populations enough to allow them to cross the fitness valley
• ... A new phenotype/species arises

• Inspired many studies
• Empirical evidence often supports one + phases,but never all three
• - chromosomal evolution (underdominance)
• - Müllerian mimicry in butterflies (alternative equilibria/multiple optimal phenotypes)
• - Mating systems in plants (alternative equilibria)

*** to the best of my knowledge

SBT is still a hot topic!

• Most populations large and outbreeding with three mating types
• Small populations in marginal habitats lose mating types as a result of drift
• Many of these populations evolve self pollination ... and small less showy flowers

• Changes in the environment likely change fitness landscapes
• Populations occupying former peaks may now occupy valleys
• "Real evolution may look less like an attempt to evolve uphill on a static landscape, and more like an attempt to keep one's footing on an ever-morphing landscape" Orr 2009

• 3 questions:
• Plausibility
• Importance in evolution
• Heuristic value

• Whitlock and Philips|:
• - "adaptive landscape" commonly invoked
• - SBT has driven many studies
• - --> greatly enhanced understanding of:
• - drift
• - population structure
• - epistasis

• I. evolution of continuous traits
• II. evolution of correlated traits
• III. genetics of adaptation

• 1. Polygenic traits
• 2. Quantitative genetics
• 3. Responses to artificial selection
• 4. Measuring natural selection

• Explaining inheritance & evolution of continuous traits was a big challenge
• Apparent blending inheritance?

Mendel's laws can be extended to multiple loci (many loci can make it look like continuous traits)

Additive polygenic model: each gene contribute relatively equal effects. The effects of each allele are additive.

Continuous variation also reflects the environment

• Statistical method of partitioning variation in polygenic traits
• Plant and animal breeding
• Powerful
• - describes inheritance
• - predicts selection response

Theory based on additive polygenic model

Vp = VG + VE + (VGxE)

VG also has multiple components = VA + VD + VI

Heritability estimates resemblance between relatives

h² = VA/VP = slope

• e.g. Galapagos finches
• h² > 0.9
• Parental phenotype predicts offspring phenotype
• Therefore, variation in beak depth is heritable

• e.g. Height of genetics I students in comparison to mid-parent height
• Females slope = h² = 0.89
• Males slope = h² = 0.81

• Response to selection depends on:
• - Strength of selection
• - Heritability = additive genetic variation/total phenotypic variation

R = ΔZ = h²S

• e.g. 6-week weight in mice
• 10 generations
• 6 replicates in each direction
• Realized h^2 = total R/cumulative S

- Increase in weight more than decrease in weight (likely physiological lower limit)

• e.g. Zea mays (corn)
• 103 generations
• selected for extremes of seed protein and seed oil
• Selection response sustained in high and reverse lines
• Selection response less in low line - biological limits?

Selection for friendliness toward humans (1959...)

• Direct responses
• - Approachability (gen 2)
• - Tail wagging (gen 4)
• - Whimper and permit handling (gen 4)
• Follow and lick humans (gen 6)

• 1. Most traits respond quickly to selection
• 2.Mutation provides genetic variation for indefinite divergence
• 3. Natural selection may oppose artificial selection
• 4. Selection most efficient in large populations

• Thresholds for survival or reproduction (truncation selection) uncommon in natural populations
• Fitness is often a continuous function of a given phenotype

• 1980s
• - Arnold, Wade, Lande
• - Applied quantitative genetic theory to natural populations

• β = selection gradient:"the slope of the relationship between fitness and phenotype for a given trait"
• Slope = β
• S = βV_PZ

• R = ΔZbar = h²S 
• R =ΔZbar = V_AZβ

• Stabilizing
• Directional
• Disruptive

e.g. Birthweight in humans is stabilizing

• Until mid 2000s unknown
• Several recent surveys suggest variation may be frequent - recall Galapagos finches

• ...Mason Kulbaba, PhD research
• Polemonium brandegeei
• Traits associated with both hawkmoth and hummingbird pollination
• Hawkmoth and humming bird abundances vary from year to year

With Hummingbird pollination - female surface exserted = approach herkogamy

With Hawkmoth pollination - female surface recessed = reverse herkogamy

• Experiments measuring selection of number of seed over stigma-anther separation (mm)
• 2012 β = -1.05
• 2013 β = 0.910

• Purple loosestrife
• Native to Europe and Asia
• Introduced to Eastern seaboard of USA in 1800's
• Aggressive wetland invader
• Dense stands degrade habitat for birds. insects and native plants
• Can clog irrigation canals and degrade farmland

• Colautti and Barrett 2013 
• - Reciprocal transplant experiment at southern, central and northern latitudes

Highest fitness in "home" environment

Mean size and age at flowering optimal for home environment

Stabilizing selection within environments

• Directional selection often strong
• Selection on mating success strong and may be stronger than selection on viability
• Temporal and spatial variation in selection gradients - how common?

• 1. Correlated traits
• 2. Multivariate selection response
• 3. Long term effects

• Many traits influencing fitness are genetically correlated with other traits
• - linkage
• - pleiotropy

Correlated traits cannot respond independently to selection

• Need to consider genetic covariances (correlations are standardized covariances)
• e.g. finch parent's beak depth and offspring's beak width

• G = genetic variance - covariance matrix
• V_i = V_A for trait i
• C_ij = COV_A for traits i and j

• Single trait: R = h^2S
• Multiple correlated traits: R = Gβ

• Multiple regression of w (fitness) on traits
• e.g. beak depth and width
• ω = a + β₁Z₁ + β₂Z₂ + e

Overall selection response is dependent on the selection pressures (positive and negative correlated) If negative correlated, the selection response will be an intermediate of the two desired traits, or closer to the trait that is undergoing stronger selection pressure

• Genetic covariances seem to influence evolution of long periods of time (1.3my in birds)
• May slow evolutionary responses or cause traits to temporarily evolve away from the optimum values
• Mutations with large effects on the phenotype may cause changes in the G matrix

Schluter 1996

• 1. Fishers geometric model
• 2. Experimental evidence with microbes
• 3. DNA sequences for specific traits
• 4. Genetic mapping (QTL mapping)

*last three are empirical evdience

• Population genetics:
• - Few known genes
• - Alternate alleles --> discrete phenotypes

• Quantitative genetics
• - Many unknown genes
• - Each allele has small, additive effects on phenotype
• Use resemblance between relatives (h²) to predict response to selection

• 2 extremes of a continuum
• What type of genes are important?

• When will mutations be beneficial?
• (figure of geometric circle within each other with a bulleyes optimum phenotype and dot of where we are in evolution, and lines showing where mutations will take us)

• Mostly when they are of small effect
• (figure of negative exponential graph with beneficial effects y axis, effect on phenotype on x axis)

Assumes populations are close to optimum

• Fisher's model and assumption that populations are close to the optimum phenotype prevailed for many decades
• Genes of small effect thought to be most relevant for adaptation
• 1980's onwards - experimental evidence accumulated...

• Nutrient poor medium
• Fitness dependent on cell size

Figure shows: sudden jumps up in cell size over generations

• e.g. MC1R mutations affecting hair and feather colour
• Mice in the Arizona desert(light rocks and lava areas)

*MC1R also affects: other mammals and birds

• But...
• - hair colour shows continuous variation
• - suggests other genes are involved

Microbes: adaptation to experimental conditions suggest that mutations of large effect may be important

• DNA sequences: 
• - A few nucleotide changes can have large effects on the phenotype
• - Key genes important across many species

• Typical or a subset of traits?
• Need to estimate genetic basis of continuous traits
• - How many genes?
• - effects on the phenotype?

... Genetic (QTL) mapping

Quantitative trait locus = physical location on a chromosome that influences a quantitative trait

• Spans many nucleotides
• Contains 1 or more of the genes controlling the trait

• Can use genetic linkage maps to estimate
• - position and number of QTL (genes) controlling quantitative traits
• - size of effect on phenotype

Look for linkage (statistical association) between genetic marker and phenotype

Recall linkage mapping (2 & 3 point test crosses)

• Genetic markers
• - can make a map of each chromosome
• - can make maps for wild species

1) Generate genetic map using markers 

• 2) Match phenotypes in segregating (F2) population to marker loci
• - Individuals with marker D from species 1 would have a phenotype more similar to species 1
• - Individuals with marker d from species 2 would have a phenotype more similar to species 2

Floral traits in 2 species of Mimulus

Crossed species and constructed linkage map

• In F2 measured floral traits related to:
• - pollinator attraction
• - pollinator reward
• - pollinator efficiency

Looked for association between markers and floral traits

• LOD Scores
• LOD = logaritm of the odds
• Indicates the likelihood that a locus controlling a quantitative trait is at a particular position along the chromosome

• Most QTL's explained <20% of variation
• 9/12 traits had 1+ QTL that explained >25% of variation

• 2 QTL had striking effects on phenotype
• yup controlled carotenoids in petals
• - LL, LC = no carotenoids, pink flowersar
• - CC = carotenoids, orange-red flowers

• Nectar QTL: 41% of variation in nectar volume
• - additive inheritance

• Colosimo et al. 2004
• 1 locus (A) explains most variation in plate number
• "Modifier" genes with small effects on phenotype also contribute to variation

• QTL studies
• - More QTL of small than large effect
• - but QTL of large can be very important ecologically

• Experimental evolution with microbes
• - Mutations of small effect more likely to be beneficial
• - Mutations that are fixed early have larger fitness effects than those fixed later

• DNA sequence analysis
• - Changes in a few nucleotides can have large effects on the phenotype
• - Key genes important across many species

Was Fisher wrong?

• Inheritance described by resemblance between relatives (h², VA, COV_A)
• Allows quantitative predictions about responses to artificial and natural selection
• Genetic covariances can constrain (or accelerate) selecction responses
• Current data indicate that adaptation involves both genes of large and small effect on the phenotype
• NB: migration, drift and non-random mating apply similarly to Mendelian and quantitative genes

• I. Introduction
• II. Evolution of sex
• III. Sexual selection
• IV. Life-history evolution

• 1. Definitions
• 2. Non-adaptive variation
• 3. Demonstrating adaptation
• 4. Comparative method

Noun (trait):  trait that increases the fitness of ind. possessing it compared to those that do not

Verb (process): change in allele freq. that incr. mean fitness

• Major focus of evolutionary biology
• Often remarkable fit between organisms and environment
• ... or between organisms that interact with one another

• Direct effects of environment
• Genetic drift
• - random changes in allele frequency due to sampling error
• Multiple adaptive phenotypes
• - camouflage in grouse chicks

• Laws of physics or chemistry
• - flower colour in Hydrangea changes with pH

• Trade-offs:
• - time is finite
• - resources (energy, water nutrients are finite)

• Pleiotropy
• - one gene affects >1 trait
• - selection on one trait causes change in a second

Developmental constraints

• What is the function of the trait in a focal organism?
• - e.g. Hooks on pigeon beaks reduce parasite loads?

• Do similar traits fulfill the same function in multiple species?
• - birds of prey

Did the trait originate for its current function?

Is the trait maintained by natural selection or merely inherited from ancestors?

• goal:show that trait developed or is maintained through natural selection
• Type of study: experimental, observational, and theoretical
• Level of study: population or comparative (among species)

• Good experiments:
• - test the effect of changes in a single trait on fitness or component of fitness
• - Control for direct effects of manipulations
• - Test several hypotheses that may explain trait function

• Good observational studies:
• - use natural variation to test alternative hypotheses
• - measure potential confounding variables
• - Require detailed information about natural history

• Consider benefits and costs of contrasting phenotypes
• Assign numerical values to benefits and costs ... or define relationship between trait value and benefit
• Use mathematical approaches to predict the best phenotype under a given set of conditions
• Examples in population genetics, and life history evolution

• Each species is a data point
• Usually observational
• Greater generality than single species studies
• Greater potential for confounding factors

• Test for association between trait and environment or
• Correlations among traits
• - Are succulent stems an adaptation to dry environments?
• - Do carnivores have larger home ranges than herbivores?
• - Do asexual plants invest less in traits that attract pollinators?

• Widely used
• Potential problem: closely related species may resemble one another due to shared inheritance of traits rather than because they experience similar selection pressures
• Can use phylogenetic information to resolve

• e.g. Are large seeds an adaptation for living in shady habitats 
• examine 12 species
• Phylogeny 1: seed size and habitat each only changed once --> not strong support

• Phylogeny 2: Changes in seed size are consistently associated with changes in habitat --> stronger support
• - 6 "sister species comparisons"

• Phenotypic resemblance due to shared ancestry (phylogeny) is accounted for by examining evolutionary change since a common ancestor
• a) sister species comparisons
• - Require many species, frequent independent changes in hypothesized causal variable (e.g. habitat type)
• - Only involve comparisons of living species
• b) Phylogentically independent contrasts
• - Compare changes in causal variable with changes in dependent variable
• - Often involves estimation of ancestral phenotypes

Hypothesis: increases in social group size should correspond to greater testes size (because males in larger groups will experience greater sperm competition)

- Need to eliminate possibility that apparent association between these traits is a coincidental result of shared ancestry

Use Phylogenetically independent contrasts (PICs) --> can change interpretations

Back to sm and lg seed example

• Only one evolutionary association
• But...
• Selection may maintain association between large seeds and shady habitats
• "Phylogenetic niche conservatism"

• Discrete or continuous traits
• Imply perfectly known phylogeny
• Imply accurate reconstruction of ancestral phenotypes
• Assume similarity among relatives is not maintained by natural selection

Interpret with caution!

• 1. Paradox of sex
• 2. Long-term advantages
• 3. Short-term advantages
• - temporal and spatial variation, mutation elimination

• Sexual --> new genotypes
• - Mating types
• - Male and female

• Asexual --> clones
• - Vegetative propagation
• - Apomixis, parthenogenesis

Asexual females have a 2-fold transmission advantage = "cost of males"

• Assumptions:
• 1) Sexual and asexual females produce same number of offspring
• 2) Reproductive mode does not affect offspring survival

• Sex predominant
• Most asexual lineages recently evolved
• Complete asexuality --> extinction

• Weismann 1889 - sex provides variations
• - species-level (long-term) advantage

...But what prevents asexual organisms from invading in the short term?

• Many theories, some evidence
• Theoretical explanations are not mutually exclusive

• All assume recombination and selection
• - Decr. freq. of non-optimal genotypes
• - Incr. freq. of superior genotypes

a) Temporal fluctuations in selection pressures

b) heterogeneous environments (spatial variation in selection pressure)

c) Eliminating mutations

• - fluctuating optima for polygenic traits- sex continually generates new phenotypese.g. beak depth in Galapagos finches
• - Avoidance of parasites/disease
• - Sex continually generates new phenotypes
• - "Red Queen Hypothesis""You must run as fast as you can if you want to stay where you are. If you want to get anywhere, you have to run faster still."
• NB: an independent Red Queen Hypothesis has been posed to explain species longevity

• b)
• Lottery model
• - offspring disperse into various patches
• - sexual female: many different tickets-
• - asexual female: many copies of 1 ticket

Asexual taxa often often in biotically simple environments

• Sibling competition- genotypes differ in resource use
• - diverse offspring compete < identical offspring

- Tangled bank" hypothesis: more genotypes can co-exist when occupying slightly different niches

• e.g. grass Anthoxanthum odoratum
• - Single genotype
• - Diverse genotypes (increase growth, and aphid resistance)

• i) Muller's ratchet
• - Forward mutations are much more frequent than reverse mutations
• - Asexual offspring inherit all existing mutations and may experience additional mutations
• - Mildly deleterious mutations accumulate in small clonal populations over time
• Multiple mutations eventually have a drastic effect on fitness

• ii) Mutation threshold
• -(A). Fitness is severely reduced in individuals with more mutations than a threshold number. Mutations are most rapidly eliminated when they occur with other mutations
• - (B & C). Before selection, sexual reproduction recombination generates a wider range of mutations per individual than does asexual reproduction

• 1. Evolution of females and males
• 2. Sexual selection
• a) male-male competition
• b) female choice
• c) sexual selection in plants

• Isogamy: Gametes with identical morphology
• ⇓ 
• Mutation affecting size
• ⇓
• Anisogamy --> functional divergence
• - large and small gametes

• fitness = offspring number x offspring survival
• Large gametes have higher survival capacity
• Small gametes produced in higher numbers
• Theory predicts association between mating types and gamete types

"Selection on mating success"

May oppose viability selection, but is still a component of natural selection

Females and males invest unequally in each offspring

• "Batemans principle"
• - Male fitness is usually limited by number of mates; therefore males will usually compete for mates
• - Females fitness us usually limited by resources; therefore females will usually be choosy

1) Combat: could explain size dimorphism, antlers, horns, etc.

2) Sperm competition: increases in group size cause increases testes size

Males often have elaborate mating displays

• Experiment on red collared widow birds
• Treatments: control; short tail (clipped)
• Monitored: body condition (mass); territories; female nesting

• Short treatment
• - better body condition
• - similar territories
• - fewer active nests (third of the mates the controls had)

• CI = contemporary industrial
• HE = historical european
• AP = african polygynous

• Strength of selection
• AP > HE > CI

• Male with better genes
• Resources (copulation gifts)
• Sexy sons

May exaggerate a pre-existing sensory bias

• Male fitness limited by access to mates, often through "pollinator choice"
• Female fitness:
• A) May be limited by resources
• - Attractive structures interpreted as "mostly male" = floral Batemania
• - Some support for "mostly male" hypothesis from species with separate sexes

• B) May be limited by pollen
• - attractive structures could influence both female and male fitness
• - changes in pollinator abundance may make this situation more common

• Male fitness highest when pollinators do not remove all pollen in a single visit
• - Staggered flower maturation
• e.g. Polemonium occidentale (separate female and male phase)
• - Staggered anther maturation
• - Staggered pollen dispensing

• cranberries, tomatoes, potatoes, eggplant
• Dodecatheon -shooting stars

• Life histories
• Rate of living
• Mutation accumulation
• Trade-offs

First three are hypotheses to explain lifespan

"Components of lifetime survival and reproduction"

• Combine to determine lifetime reproductive success (fitness)
• Much variation in:
• - lifespan
• - reproductive cycles
• - size and number of offspring

• e.g. Century plant (blooms every several decades)
• Why?

• "Darwinian Demon"
• - reproduce at a birth
• - infinite life span
• - infinite reproductive episodes
• - large numbers of viable offspring

Finite time and resources --> trade-offs

"You can't do everything at once"

• Function: 
• - growth
• - reproduction: offspring number and size

• Resource investment in each function reflects:
• - total resources
• - trade-offs
• - allocation hierarchy

• Why do organisms age and die?
• Rate of living theory
• "Evolutionary" theory

• There is a physiological limit to cell and tissue repair
• Short life, high metabolic rate/ cell division vs. Long life, low metabolic rate/cell division
• Prediction: selection should place populations at physiological limit

• ...but
• Drosophila studies: artificial selection can increase lifespan without significant changes in metabolic rate
• more explanation required

NB: not mutually exclusive

• 1) Mutation accumulation
• - Late-acting deleterious mutations accumulate because selection becomes weaker with age

2) trade-offs between reproduction and repair

• a) Wild type matures at age 3, dies at age 16; prior to age 16, annual rate of survival = 0.8
• b) mutation that causes death at age 14; prior to age 14, annual rate of survival = 0.8

• W_wildtype = 2.419/2.419 = 1.0
• W_shortlife = 2.34/2.419 = 0.97

• Deleterious mutations that act late in life will accumulate because selection against them is weak
• e.g. genes causing cancer, Huntington's, Alzheimer's

If true, inbreeding depression should incr. with age

Studies of fruit and house flies support mutation accumulation, also biennial plants

• Mutation incr. early reproduction and causing earlier death
• c) mutation that causes maturation at age 2, death at age 10, annual rate of survival = 0.8

... even at the expense of lifespan

• Phenotype        Lifetime RS    Fitness
• Wildtype               2.419          0.91
• Short-lived            2.34           0.90
• Shortest lived,       2.663          1.0
• early reprod.

• Until recently, most evidence in phenotypic costs of reproduction
• Incr. reprod. reduces subsequent growth and survival in many animals and plants
• e.g. clutch size in birds; seed set in plants, investment in ovaries in fish

• Recent work has id'd specific genes, e.g. Drosophila
• "Methuselah allele" - increases resistance to starvation, heat, and a herbicide but reduces reproduction in early life

• a) Intrinsic factors:
• -accumulation of late acting deleterious mutation
• - trade-offs between reproduction and repair

...but when does selection favour a long versus a short life??

• b) Extrinsic factors:
• - predation, disease, resource depletion

• Mainland populations experience higher predation than island populations
• Other conditions similar

• Mainland:
• - early reproduction higher than in island
• - Reproductive output declines with age
• - Stiffness (aging) of connective tissue occurs at a higher rate in mainland females

• Strength of natural selection decr. over life-span
• - accumulation of late-acting deleterious mutations
• Trade-offs between reproduction and survival
• Logic of trade-offs applied to many aspects of life history
• - reproductive effort
• - mate attraction versus gamete production
• - offspring size and number
• - reproduction versus defense

• Australopiths with suite of traits that may have improved fighting ability, including hand proportions that allow formation of a fist
• Bones in part of skull that suffer highest rates of fracture in fights show greatest increase in robusticity during hominin evolution and show greatest difference between males and females
• Bipedal posture also improves fighting performance

• Scopes Monkey trial
• In 1925, Tennessee schoolteacher John Scopes was convicted of violating new state law prohibiting teaching of evolution

• In 1995, Alabama state board of education ruled that all textbooks discussing evolution must carry disclaimer stating that evolution is theory, not fact
• One school board member: "Most people do not believe that we descended from apes"

• Scientists universally agree that humans belong to the same clade as apes
• Includes gibbons (SE Asia)
• Great apes (Hominidae):
• - Orangutan (SE Asia)
• - Gorilla (Africa)
• - Chimpanzee (Africa)
• - Bonobo or pygmy chimp (Africa)

Numerous synapomorphies distinguish apes from other primates (e.g. large brain, no tail, more erect posture, differences in limb)

• i.e. Gorilla, chimp, bonobo (not monkeys)
• First suggested by T.H. Huxley (1863)

• Apes = Hominoidea
• Great apes = Hominidae
• African great apes = Homininae

• Humans are apes (African great apes) in the same way that birds are dinosaurs
• They are paraphyletic taxa without humans and birds, respectively

• Synapomorphies include:
• - elongated skulls
• - enlarged brow ridges
• - shortened but stout canine teeth
• - enlarged ovaries and mammary glands
• - reduced hairiness

• Supported by molecular evidence (Sarich and Wilson 1967)
• Used molecular clock, calibrated with fossil record (apes and Old World monkeys diverged 30 Ma)
• To suggest that humans and other African great apes shared ancestry ca. 5 Ma

• Relationship among African Great Apes not resolved by earlier phylogenies
• One of the four possible scenarions

Decades of debate due to conflicts between different traits, different data sets

• e.g.knuckle-walking (on middle of three bones in each finger) is a shared, derived trait in gorillas and chimps
• Characterized by specialized hand and wrist anatomy
• Absent in humans

• Derived in African great apes because Asian great ape (orangutan) walks on fists (on finger bones closest to hand)
• Knuckle-walking tends to evolve when fingers are specialized for tasks other than ground locomotion

• Considered alone, most parsimonious explanation is that humans diverged before evolution of knuckle-walking
• i.e. gorillas and chimps are sister taxa

• But not parsimonious if other traits considered
• e.g. synapomorphies in chimps and humans re: features of teeth, skull, limbs, external genitalia

• If chimp and gorilla share closer common ancestor:
• - In each case, ancestral traits independently lost in gorilla
• - Or each derived trait gained independently in chimp and human

• Recent fossil evidence suggests that human evolved from knuckle-walking ancestor
• And secondarily lost trait

Therefore, consensus that Fig. 20.3a best characterizes phylogeny of great apes

• But consensus slow in forming
• Because also conflicts among molecular data sets

• Most support human-chimp sister group theory (Fig. 20.3a)
• e.g. Ruvolo et al. 1994
• Using COII

However, "persisten" minority of analyses placed gorillas and chimps (Fig. 20.3b) or even gorillas and humans (Fig. 20.3c) as sister groups

• e.g. Barbulescu et al. 2001
• - Retrovirus insert in genome of both chimps and gorillas
• But same locus in humans lacks insert and appears never to have had it (cf. SINEs and LINEs)
• Suggests that humans diverged from lineage that would give rise to gorillas/chimps before latter acquired insert
• i.e. that Fig 20.3b correct

• Molecular phylogenies are "gene trees" (showing evolutionary history of gene)
• Not "species trees"
• Infer species trees from gene trees but not always the same thing

• e.g. mtDNA may be misleading if hybridization 
• e.g. Numts
• e.g. differential loss of ancestral alleles due to selection or drift

• Gorilla ancestor inherits alleles 1,2,4
• Chimp/human ancestor inherits alleles 3,5,6,

• In gene tree
• - 2,3 most similar
• - 4,5 most similar

In Specie tree, human/chimp siter to gorilla

• If second speciaion event (human/chimp) in close succession: Gorilla (allele 2) and chimp (allele 3) would appear most similar
• OR: If gorilla inherited only allele 4
• - Gorilla (allele 4) and human (allele 5) would appear most similar
• -"sampling effect"

gene tree ≠ specie tree

• Reconstruct phylogenies with many independent genes
• Ruvolo (1997): 14 independent data sets
• - 11 showed human/chimps as sister groups
• - 2 gorilla/chimps
• - 1 human/gorilla

General consensus that chimps our closest living relative

• Grehan and Schwartz (2009) say orangutan our closest extant relative (not chimp)
• Also behavioural similarities according to Schwartz:
• - Orangutans "study a situation and learn through observation before putting a plan into action"
• - Whereas chimps and gorillas "tend to lose their cool and resort to brute force and sometimes hysteria when confronted with a puzzle"

But colleague says: "I think he is utterly, factually wrong"

• General consensus that chimps are our closest living relative
• BUT we're not directly evolved from common chimp-human ancestor
• - Many other genera along the way (e.g.  Australopithecus, Afropithecus, Kenyanthropus, Parathropus)
• - And other species in genus Homo

Homo genus diverged from the australopithecines about 2-2.8 million years ago in Africa

• At least 6-8 other Homo species proposed
• Although debate whether some distinct species or regional variants of each other
• 1. H. habilis
• 2. H. erectus
• 3. H. ergaster
• 4. H. antecessor
• 5. H. heidelbergensis
• 6. H. neanderthalensis
• 7. Denisovans
• 8. H. floresiensis?
• 9. H. sapiens

• 2.4-1.4 MA
• Made tools (discovered by Louis Leaky, named "handy man")
• Considered Australopithecus by some
• - primitive cranial morphology
• - Arboreal habits rather than bipedalism

• 1.8 Ma - 70,000 years ago
• First discovered on Indonesian island of Java
• Most famous = Peking Man
• First human to walk truly upright
• - evolution of locking knees
• - different location of the foramen magnum
• May have used fire to cook their meat

Sometimes considered non-Asian variant of H. erectus rather than separate species

• Human evolutionary tree more bushy than thought
• Two extinct hominids overlapped in time in the same area

• Fossils found in 2000 by Maeve Leakey in Kenya create "messy kink in the iconic straight line of human evolution with its knuckle-dragging ape and briefcase-carrying man"
• Evidence that Homo habilis and Homo erectus lived side-by-side about 1.5 million years ago (for at least half a million years)

• Probably didn't interact with each other:
• - H. habilis likely more vegetarian
• - H. erectus likely ate some meat

• Skulls from Homo erectus showed that females were much smaller than the males
• Suggests polygamy:
• - Primate species with same-zed males and females tend to be more monogamous (e.g. gibbons)
• - Species that are not monogamous have much bigger males (e.g. gorillas and baboons)

• ca. 780,000 - 980,000 years ago
• Suggested as common ancestor of Neanderthals and modern humans (H. sapiens)

• Archaic Homo made early trip to Europe
• Spanish remains of Homo antecessor 400,000 years older than previous record

• Previous evidence of human activity in Spain, France, and Italy around 1 million years ago but no human remains, only animal bones and stone tools
• Ancestor of Neanderthals and modern humans?
• Scientists generally agree that modern humans spread out of Africa starting about 50,000 years ago (later)

• Heidelberg Man
• ca. 800,000 to 300,000 years ago
• Also proposed as H. sapiens heidelbergensis

• Now generally considered last common ancestor to H. sapiens and H. neanderthalensis 
• Stringer (2012) Evolutionary Anthropology

• ca. 250,000 to 24,000 years ago
• Discovered in 1856
• Also proposed as Homo sapiens neanderthalsis

• mtDNA suggests no significant gene flow between H. neanderthalensis and H. sapiens
• But nuclear genome suggests some interbreeding (Green et al. 2010)
• Shared common ancestor about 660,000 years ago

Red-headed neanderthals may have existed. Study points to unique genetic variant

• DNA from remains of two Neanderthals
• Found variant of MC1R which would produce red hair
• - different variant than present in modern human redheads
• - independent evolution

• Would be correlated with pale skin
• - Selection for lower levels of sunlight in Europe
• - Less need for protection against strong UV radiation
• - And able to generate more vitamin D

• An international team of scientists has identified a previously "shadowy" human group known as the Denisovans as cousins to Neanderthals who lived in Asia from roughtly 400,000 to 50,000 years ago and interbred with the ancestors of today's inhabitants of New Guinea
• DNA extracted from broken finger bone and wisdom tooth yielded sequence of complete genome
• Showed that the genome of people from New Guinea contain 4.8% Denisovan DNA

• mt genome showed Neanderthals and modern humans to be sister taxa (Krause et al 2010)
• But nuclear genome supports Neanderthal-Denisovan sister relationship (Reich et al. 2010)
• Scientists propose that the ancestors of Neanderthals and Denisovans emerged from Africa 500,000 years ago
• - Approx. 50,000 years ago, they interbred with modern humans expanding from Africa along the coast of South Asia

No clue yet what they looked like (apart from wisdom tooth being very different from both Neanderthals and modern humans)

• "Hobbits"
• Discovered on Indonesian island of Flores in 2003
• ca. 1m tall, with brain about the size of a chimpanzee's
• Fossils from ca. 100,000 - 18,000 years ago
• But no consensus as to whether distinct species or stunted modern humans

• Doubt cast on Hobbit hominids from Flores Island
• Australian team claims dwarfism caused by malnutrition could explain "Homo floresiensis"

Dr. Peter Obendorf: Severe iodine deficiency in pregnancy can cause people to grow little more than a metre tall with bone characteristics very similar to those of the Flores hobbits

• Dr. Peter BROWN (one of researchers who discovered the remains):
• - "Sheer speculation"
• - "The authors have not examined the original fossil, have little and no experience with fossil hominids..."

• Genetic data would clarify the evolutionary relationship between the Hobbit (H. floresiensis) and modern humans
• But none obtained to date
• - Poor preservation
• - Extensive contamination by modern human DNA

One more Homo species? 3D-comparative analysis confirms status of Homo floresiensis as fossil human species

Flores bones show features of Down syndrome, not a new 'Hobbit' human

CONTENTIOUS/HOTLY DEBATED

• Famous hoax consisting of fragments of a skull and jawbone collected in 1912 from a gravel pit at Piltdown in England by Charles Dawson
• Eoanthropus dawsoni
• Considered "missing link" and "the first Englishman"
• - suggested that the British Isles had been an important site of early human evolution

• Not (definitively) exposed as forgery until 1953
• Modern human cranium and orangutan jaw with filed-down teeth

• From ca. 250,000 years ago to present
• All humans today classified as Homo sapiens sapiens
• H. sapiens would have overlapped with H. neanderthalensis 
• Recent evidence of some interbreeding 

• Most paleotologists agree that modern humans are descendants from the H. ergaster/H. erectus  groups
• But still "working out" details of how and where

• three models
• a) African Placement model
• b) Multiregional model
• c) Hybridization and assimilation model

• Modern H. sapiens evolved in Africa ca. 250,000 - 200,000 years ago
• Began migrating from Africa 70,000 -50,000 years ago
• - Hence also called "Out of Africa" model

Eventually and completely replacing existing Homo species in Europe and Asia

Speciation and then migration --> completely replaced local, archaic humans

• Homo sapiens evolved as one interconnected species in Africa, Asia, Europe (some gene flow between regions)
• Gradual transformation(in each location) from archaic to modern humans through combination of migration and mating

Migration then speciation --> local, archaic humans evolved into modern humans

• "Out of Africa" model (i.e. origin of Homo sapiens in Africa with recent migration out of Africa)
• But with occasional hybridization between modern and archaic humans "as they pushed into new lands"
• Speciation and then migration --> mostly replaced local, archaic humans but with some interbreeding first

Most evidence supports "Out of Africa" model but not necessarily "African Replacement" model

• 1. Homo sapiens monophyletic
• - Phylogenetic analysis using multiple morphological characters, showed that all modern humans are more closely related to each other than any is to local, archaic species
• - DNA sequences data (mt and nuclear) also show modern humans to be monophyletic

Greater genetic diversity within African populations of Homo sapiens

• Out of Africa model predicts that alleles present in Europe and Asia are subsets of those in Africa (if Homo sapiens evolved in Africa and then migrated outwards)
• - Tishkoff et al. (1996) genotyped > 1600 people from 7 geographic regions
• - As predicted, African populations show much greater allelic diversity than on-African populations
• - Number of alleles decrease with distance from sub-Saharan Africa

Genetic differences among regions small, indicative of recent divergence

• Most recent common ancestor of all modern humans approx. 172,000 years ago; of all non-Africans approx. 52,000 years ago
• Low intraspecific diversity in humans compared to most species

• Genetic homogeneity also compounded by recent bottleneck?
• e.g. "Toba catastrophe"
• - Supervolcanic event (50 times greater than the 1980 eruption of Mount St. Helens)
• - At Lake Toba on Sumatra 70-75 ka
• - Reduced population to 10,000 (or ca. 1,000 breeding pairs)?

• Genetic differences at neutral loci do exist, but very subtle
• Adaptive traits are a very small component of the overall human genome
• - Have arisen primarily as the result of small groups of people moving into new environments
• But include very noticeable characteristics such as skin, hair and eye colour, body shape, etc.
• Have selective advantages in different climates

And, as humans, we're able to perceive difference more than we could in other species

• we evolved to look unique
• More genetic variation in genomic regions that control facial characteristics than in other areas of the genome

• Natural selection has altered the appearance of Europeans over the past 5,000 years
• "Paler skin permits more efficient manufacture of vitamin D, but eye, hair colour more important for sexual selection (indicating group affiliation) than adaptation to environment?"

• e.g. evidence for anatomical continuity between archaic humans and modern humans from those regions
• Likely due to convergent evolution or hybridization

• Diagnostic features of modern H. sapiens but with features characteristic of earlier human species, such as relatively large front teeth
• -Dr. Erik Trinkaus: "The question is where did they get them from? Either they re-evolved them, which is not very likely, or to some degree, they interbred with archaic groups. Sex happens. I find this neither disturbing nor surprising."

Aside: single toe bone found suggests individal wore shoes

• Suggests hybridization between modern humans and Neanderthals shortly after modern humans left Africa
• - Reich et al. 2010 estimated 2.5% of genome of non-African modern humans is derived from Neanderthals

• And hybridization between modern humans and Denisovans when ancestors of today's Melanesians were crossing Asia (after already hybridizing with Neanderthal)
• - Reich et al. 2010. estimated additional 4.8% of genome of Melanesian is derived from Denisovans

• Consistent with model between replacement and hybridization and assimilation
• --> "Leaky replacement"

Cross-breeding boosted Homo sapien's ability to cope with cool climates, but the hybrids may have had trouble breeding

• Chimps make and use simple tools
• e.g. strip stems and twigs off leaves to fish termites out of mounds
• e.g. use leaves as umbrellas
• e.g. use rocks and stick to hammer open nuts

• Other animals as well
• e.g. one of Darwin's finches used cactus spines to extract insects from bark

Using complex tools is what distinguishes humans

• Earliest complex tool ("Oldowan tools") found from 2.5 Ma
• - 2.6 Ma in Ethiopia:
• - Sharp-edged stone flakes and handheld chopping tool 

• No definitive evidence that any Homo species had appeared that early
• Oldest reliably date Homo fossil 2.3 my old upper jaw (but also from Ethiopia)

• Or perhaps used by Paranthropus?
• Co-existed with early Homo in same part of Africa over this approx. time span

• Susman (1994) argues that Paranthropus made and used tools
• Based on thumb anatomy

• Humans have 3 muscles in thumb that chimps lack
• Along with thicker metacarpals
• - Which make human hand more adept as precision grasping
• - Likely evolved in response to selection pressures for manufacture and use of complex tools

• Relative thickness of thumb metacarpals in H. neanderthalensis, H. erectus, and P. robustus also greater than in chimps
• Australopithecus afarensis (that disappeared from fossil record before Oldowan tools appear) is like chimp

• Controversial
• General consensus is that early Homo is responsible for most if not all Oldowan tools
• - Whenever tools found in association with hominin fossils, Homo is always there but Paranthrops may be absent

• A. Brain size and anatomy
• - Part of brain involved in human language include: Broca's area and Wernicke's area

• - Tobias (1987): casts of insides of braincases of H. habilis show large brain with clear enlargements of Broca's and Wernicke's areas
• -Suggests at least rudimentary language in H. habilis
• i.e. language may be as much 2 my old

• B. Larynx
• - Spoken language requires modifications to larynx
• - In modern human newborns (and in other mammals), speech not possible:
• - Larynx is high in throat
• - Can rise to form a seal with back of opening of nasal cavity
• - Allows air to bypass mouth and throat on way from nose to lungs
• - Prevents infants from choking

• Larynx descends in human babies at ca. 3 months
• Provides more space for tongue to move
• And changes shape of resonating chambers in larynx
• - articulation greater diversity of vowel sounds

• Arenburg et al (1989, 1990):
• - 60,000 year old Neanderthal skeleton from Israel included intact hyoid bone from larynx
• - Anchor for throat muscles that, in humans, are important in speaking
• In Neanderthal, hyoid virtually identical to humans and very different from chimps
• Concluded that they had descended larynx
• Would increase chance of choking
• - therefore suggested that it wouldn't have evolved unless it also carried a substantial benefit - i.e. speech

• C. Genetic evidence
• Krause et al. 2007
• FOXP2 gene sequenced in Neanderthal
• FOXP2 first tied to language in 2001
• - when a mutation in it was shown to affect a person's ability to speak

• Neanderthal FOXP2 showed same two mutations that the human gene carries (compared with the chimp version)
• Although only one of several factors involved in language

• D. Evidence of written language
• - Spoken language almost certainly preceded written language
• - First unequivocal evidence of written language (arbitrary symbols standardized within a culture to represent objects and ideas) found in cave paintings in Germany and France ca. 32, 000 years old (Noble and Davidson 1991)

• "His large head, with the thick frontal bones, must have been very good for butting a brother Neanderthal, but it was no use against the stone wall of advancing civilization..."
• Quennell and Quennell (1945)

• "The other humans: Neanderthals revealed" by Stephen Hall
• - Dominated Eurasia for almost 200,000 years
• e.g. Spain, Italy, Germany, France, Britain, Romania, Croatia, Russia, Uzbekistan, Iraq, Isreal, Iran
• As far east as Siberia

• Last verified evidence of them 28,000 years ago
• In cave in Spain: "embers in some of those fireplaces died out only 28,000 years ago - the last known trace of Neanderthals on Earth".

• short, stout fireplug of a physique
• - Males averaged ca. 5'5" and 185 lbs
• Females ca. 5'3" and 154 lbs
• Wide bodies conserved heat in cold climates

• Massive muscles and large rib cage, indicating high level of activity
• Typical Neanderthal male would have needed up to 5000 calories a day
• Given high energy requirements, women and children likely hunted alongside them
• Many healed fractures on upper limbs and skulls

• Most adults with heavily worn front teeth
• Brain about the same size as ours
• Red hair, pale skin, maybe even freckles

• Evidence of ornamental objects
• e.g. pierced animal teeth and ivory rings
• e.g. black pigment for body decoration

• High-resolution analysis of teeth suggests that they may have matured up to 4 years earlier than modern humans
• Teeth show daily and longer periodic growth lines
• e.g. weaning, episodes of nutritional deprivation or other environmental stresses
• Finally finish growing at end of adolescence
• Modern human child dated to ca. 160 ka showed typical onset of puberty
• But 100,000 year old tooth of young Neanderthal showed 8-year old child approaching puberty 
• What does this suggest about adult mortality rates?
• --> HIGH

Less time spent learning and developing within context of social group

• Envr. in Mediterranean reconstructed from pollen and animal remains:
• Pleasant scrub savannah 50 -30 ka
• - Evidence of rabbit bones, tortoise shells, mussels, dolphin bones, seal skeleton
• Cold, semiarid steppe by 30 -23 ka
• - Neanderthals relied almost entirely on hunting big and medium sized mammals (e.g. horses, deer, bison, and wild cattle)
• - Probably some vegetable material, but no evidence of milling stones or other tools for processing plant food

Wide climatic fluctuations, sometimes within the space of decades

• 1500 bone fragments of late Neanderthals found in cave in Spain 2000
• From at least 9 ind.
• - 5 young adults, 2 adolescents, 2 children (ca.8 and 3 yrs old)
• - well-preserved

• All showed signs of nutritional stress
• And also showed signs of cannibalism (or predation by modern humans)

• Total size of population probably never exceeded 15,000
• Suffered from shrinking range
• - "Pinned down in Iberia, pockets of Central Europe, and along southern Mediterranean"
• - And further squeezed by the westward expansion of H. sapiens

Neanderthals and modern humans overlapped starting ca. 45 ka

Probably avoided or even excluded each other but...

• Recently genetic evidence for some interbreeding
• Erike Trinkaus: "There were very few people on the landscape, and you need to find a mate and reproduce. Why not? Humans are not known to be choosy. Sex happens"

Presumably Neanderthals better adapted than modern humans for colder climate

• Were modern humans "simply more clever, more sophisticated"?
• Dramatic genetic change in brain of modern humans?
• Better technology?
• - Neanderthals with thrusting spear but lacked projectile weapons
• - Although late Neanderthal skeleton found in 1979 with "surprisingly modern repertoire of tools"

• Differences in societies
• Less "cultural buffering" in Neanderthals
• - Technology, social organization, or cultural tradition that permits 'bet-hedging'

• e.g. division of labour between men (hunters) and women and children (gatherers)
• - Spreads risk, not depended only on game
• - And not as dangerous, especially important for pregnant women and kids

• Important with changing climate
• Increases in longevity also increase intergenerational transmission of knowledge

• And Neanderthal social unit only about size of extended family
• - Larger pop. in early modern humans would provide greater mate choice selection
• - Larger pool of knowledge for transmission of survival skills and tool-making technologies
• - And prolonged adolescence would provide more time for learning and developing

• Red handprints from modern humans recently discovered on cave wall in Spain dated to ca. 20.3 to 19.5 ka (same cave where last known evidence of Neanderthals on earth 28 ka)
• "It's like they were saying, Hey, it's a new world now"