Language, complexity, and brain evolution

The role of relaxation of selectionTerrence W. Deacon - Montreal, June 2010

It is a species-unique, highly divergent capacity that undoubtedly reflects extensive evolution, and yet a huge fraction of the constitution of this highly complex adaptive behavior is contributed by social transmissionIt is ubiquitous in all activities throughout the lifetime (e.g. not just for courtship) used for diverse purposes, and is not sexually dimorphicIt is perennial paradigmatic case cited to challenge the ability of natural selection to explain complexity (e.g. Wallace to ID)

The oddity of language evolution

Language functions are complex, cognitively demanding, highly robust, and thoroughly integrated into human cognition, suggesting long evolution and intense selection on brain functionLanguage utilizes neurological substrates that are quite distinct and independent of those underlying any mammalian vocal callsIt requires a highly synergistic, phyletically atypical, involvement of diverse brain systemsand these critical brain structures are not human-specific, but originally evolved for other functions — not for vocal communication.

The oddity of language evolution

Synergy among structures evolved for other purposes

Language functions are not merely localized to discrete cortical areas. As more aspects of language are considered we are finding that many cortical and subcortical brain regions are involved.

Language processing thus involves complex synergies between multiple brain systems.

“The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me feel sick!”

The extravagant complexity problem

Darwin postulated that selection with respect to sex can explain many extravagances, even those which decrease the health and survival of their bearer.

He argued that language evolution might be compared to the evolution of complex displays, like some bird songs, and that it evolved from a courtship display—song.

— Darwin in a letter toAsa Gray, April 1860

Wallace’s doubts about complexity

Alfred Russell Wallace

"... natural selection could only have endowed the savage with a brain a little superior to that of an ape."— Wallace: Quarterly Review, April, 1869, p. 392.

Wallace also denied the validity of sexual selection because it seemed to import aesthetic psychological factors into natural selection.He was wrong about sexual selection, but its role in language evolution seems unlikely because it tends to produce divergent and complementary male / female traits, whereas both human sexes have similar language abilities.

Moving beyond lucky accidentsBut the appeal to extreme accident e.g. “hopeful monsters” to explain language is the biological equivalent of appealing to miracles.

Did a lucky genetic accident make language possible, or did language make some genetic accidents more valuable than others?

"Natural Selection is too often treated as a positive agency. It is not a positive agency; it is entirely negative ”

— J. M. Baldwin (1896)It is a subtractive process, like sculpting. It requires a generative process to produce the living forms from which to chisel away the less-well fitted and preserve the rest.The generative process is epigenesis — its mechanisms contribute constraints and biases that indirectly influence natural selection.

A complement to natural selection?

Duplication in development & evolution

1. Reproduction ... including development & learning

2. Divergence, drift, recombination3. Environment-correlated preservation

= niche complementation

1. Duplication of gene or function... including epigenetic accommodation

2. De-differentiation or degradation3. Synergy-correlated preservation

= redistribution & complexification

Inter

Inter-

orga

nism

Intra-

orga

nism

gene duplication

functional variations

different variants evolve in different lineages

reduced selection

mutations are not eliminated

= relaxed selectionIdealized single gene selection circuit

Intra-organismic replication-duplication

Hemoglobin gene duplication synergy

Spontaneous duplication of the hemoglobin gene allowed one to accumulate mutations, while function was maintained by the other. Drift in form increased the probability of “discovering” a complementary shape.

α β

Further βduplications

α and β evolve to fit

hemoglobin gene duplication

ancestral hemoglobin gene ev

olut

iona

ry ti

me

Duplication of beta hemoglobin genes (above)Expression during mammalian gestation (below)

Duplication ... functional drift ... synergySpontaneous degradation of duplicate genes produced beta- hemoglobin variants with different oxygen affinities, as well as some pseudo-genes.The problem of transferring oxygen from maternal to fetal hemoglobin offered “functional niches” that certain variant hemoglobins could fit

Duplication of genes that control the expression of suites of other genes

Evodevo: Multiple duplications of fly Homeobox genes (1) produce body segmentation. The entire Hox gene family is duplicated in vertebrates (2).

1

2 2

Functional redundancy of duplicate body parts relaxes selection on others, in which accumulated mutations produce variants of structure and function. Variant forms will tend to dedifferentiate but may also come to complement the functions of others,thus initiating selection for their synergistic effects.

= duplication of body structures

divergence complementation

• Most mammals synthesize vitamin C endogenously but not anthropoid primates, fruit bats, and many birds.

• Monkeys and apes must regularly acquire vitamin C from their diet.

When duplication is external

Human non-functional vitamin C gene

A non-functional human gene for the enzyme essential for endogenous synthesis of vitamin C was discovered by using a probe gene from rat.

The human LGO gene has accumulated many random mutations and is no longer tran-scribed (pseudogene).

Extrinsic masking factor masked function

reduced selection & degeneration

... is analogous to gene duplication in influence, but it can lead to very different consequences.

Extrinsic functional duplication

=> fragmentation & recruitment of other loci.

Extrinsic functional duplication

selection shifts to any other gene

loci that fractionally

contribute to the reliability of obtaining the extrinsic

factor

in the absence of selection mutations

accumulate producing increased individual

variants and loss of

function allowing

selection to shift loci

variants and variants and

evolutionary sequence

2. dietary 2. dietary substitution

3. dependence & 3. dependence & re-adaptation

1. Ascorbic acid not in diet = stabilizing

selection for endogenous synthesis.

frui

t acq

uisit

ion

mutationLGO genead

apta

tions

for

pseudogene

Loss of vitamin C synthesis

rhodopsin gene duplications

X

gene duplications

Color vision for ripeness detection?

gene duplications

Duplication of retinal color pigments as a vitamin C adaptation

Domestication as a source of extensive external redundancy

White Rump Munia

Bengalese Finch

wild domesticated250 years of breeding for color without the effects of natural or sexual selection resulted in more complex song, social song learning, and involvement of multiple brain regions

Increased song complexity in the absence of selection

from the laboratory of Kazou Okanoya

Primary song elements

Transition probabilities

Wild

Domesticated

a1 a2 a3 b1 b2 b3 c d e f

a1 a2 a3 b1 b2 b3 c d e f

a b c d e f

a b c d e f a b c d e f

a b c d e f

a b c d e f a b c d e f

a b c d e f

a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f a b c d e f

HVC HVC

NCM L1 L2L3

OVMld

Cochlearnuclei

mMANiMAN

X

Av

DMDLM

RA

nXII

RAcup

cochleasyrinx

redrawn fromJarvis & Nottebohm 1997

PNAS 94,4097-4102

cHV

VOCAL MOTOR AUDITORY

HVC HVC

NCM L1 L2L3

OVMld

Cochlearnuclei

mMANiMAN

X

Av

DMDLM

RA

nXII

RAcup

cochleasyrinx

redrawn fromJarvis & Nottebohm 1997

PNAS 94,4097-4102

cHV

VOCAL MOTOR AUDITORY

used byboth

used onlyby Finch

Nuclei & connections functioning in

song

connections

Simulation of relaxation effect

reduced linearity

degraded filter

increased learning role

increased variation

modified from Ritche & Kirby ’05

Is there inter-action between song structure and learning biases?

stabilizing selectiondirectional selection no selection

“mutational” noise introduced in each

generation

Innate song production involves an auditory template because

deafening results in degraded song

produce subsonglisten to self singcompare to auditory biaslearn differencemodify subsong

adult song

Innate vocal-motor biasInnate auditorysong template

Song-acquisition program

Off-loading to social transmission occurs because degradation of the

auditory template increases the influence of auditory experience

produce subsonglisten to self singcompare to auditory biaslearn differencemodify subsong

adult song

Weak vocal-motor biasDegradedsound bias

Next generation earlyauditoryexperience

Degradation = susceptibility to influence

By removing the stabilizing effects of sexual selection, constraints on song generation are degraded to the point that other neural influences can now affect song. Since auditory bias is modified by experience song structure becomes increasingly subject to social influence.

degraded control

Wild

Domestic

Offloading control to epigenetic processes increasingly opens the door to social transmission

innate-song transmitted-song

epigenesis

learning

degradedgenetics

epigenesisepigenesisepigenesisepigenesis

learninglearninglearninglearning

epigenesisepigenesisepigenesisepigenesisepigenesis

learninglearninglearninglearning

1. Reduced arousal-coupling of vocal behavior (babbling)

2. Equalization of phonological-transition biases

3. Reduction, simplification, and re-use of innate call features in speech prosody

4. Increased role of auditory learning in vocalization

5. Neurologically distributed synergistic organization

6. Increased social-cognitive regulation

Finch analogues in language?

innate call system

cortical language system

Could humans be a self-domesticated species; i.e. a degenerate ape?

The Finch analogy suggests that genetic de-differentiation affecting the nervous system may have contributed to functional complexity in human language evolution. Though, as in the case of ascorbic acid synthesis, de-differentiation is only relevant for opening the door to higher-order synergies, these can eventually come under the influence of selection because of their synergistic effects.

wild

domesticwild

domestic

3. Unmasked selection for new functional synergies drives anatomical reorganization

Relaxed selection and co-evolution both contributed

of primate limbic-midbrain control over vocal emotional communications

cross-talk involvingmany cerebral cortical systems

2. Relaxed selection allows

1. Initial state

31

Language structures selected for learnability

and ease of use

Brain functions selected for the special learning for the special learning & production demands & production demands

of language

selection pressure on language

rapid historical

change

selection pressure

on brains

slow evolutionary

change

Brains and language co-evolved

Once language-like behavior became critical to hominid life

it effectively became an artificial niche to which hominid

brains had to adapt.

... like beavers have adapted to the aquatic niche they create.

The human neural adaptation to language is analogous to beaver

adaptation to its aquatic niche

languageadaptation

symbolicculture

aquaticadaptation

dambuilding

Competitive shifts in connectivity?

Embryological divergence of brain/body proportions should affect axonal competition, favoring connections from relatively enlarged structures.

= reduced peripheral representations (left), cortical recruitment of visceral motor targets (1), prefrontal dominance (2, 4), greater cortico-cerebellar connectivity (3).

Brain size increase as duplication?

Expansion of cerebral cortex itself may have contributed to a form of neurological relaxation effect, allowing regions to partially reduce functional demand on one another, and thus analogously increase regional diversity and the probability of randomly diverging into complementary synergistic relationships. This was exaggerated by disproportional expansion of cerebral cortex with respect to thalamic, striatal, and spinal structures.

*

atg c c gatg c c gatg c c ga#c#Genetics

Epigenesis

Acquisition

Transmission

Nicheconstruction

g

constructionNiche

construction

EnvironmentFunction

Naturalselection

Distributed causality of language evolution