The parental antagonism theory

of language evolutionPreliminary evidence for the proposal

William M Brown BA MSc PhD

Human Evolutionary Behavioural Science Lab

w.m.brown@uel.ac.uk

Overview

• General perspective on social evolution

• Genomic imprinting and conflict

• Parental antagonism theory of language

• Empirical evidence

• Summary of findings

‘Out-dated’ ranked view

• Physics

• Chemistry

• Biochemistry

• Biology

• Neurosciences

• Social Sciences

• Humanities

A revised view

• So-called higher or more complex levels of

social behaviour and organisation can tell

us something about lower levels of

biological organisation (e.g., genome

evolution).

• There are social principles of evolution.

Royal chambers of termites

Division of labour societies

Ecological variability

The major transitions1. Replicating molecules -> Populations of molecules

2. Independent replicators -> Chromosomes

3. RNA as genes & enzymes -> DNA genes / protein enzymes

4. Prokaryotes -> Eukaryotes

5. Asexual clones -> Sexual populations

6. Protists -> Multicellular organisms

7. Solitary individuals -> Colonies w/ non-reproductives

8. Primate societies -> Human societies with language

Amalgamation: e.g. Chromosomes, eukaryotes, sex

multicellular colonies.

Specialization: e.g. DNA &

protein, organelles, anisogamy, tissues, castes

Obligate Symbiosis: e.g. Organelles, tissues, castes

Conflict and Mediation: Meiotic drive (selfish non-

Mendelian genes),

New Forms of Information Transmission: DNA-

protein, cell heredity, epigenesis, cultural transmission.

Hamilton’s rule

b r > c

• b: help given to recipient

• r: degree of genetic relatedness between altruist and recipient

• c: price to altruist in terms of fitness

• Formula valid for invasion and maintenance

• Applies to major transitions in evolution.

Language evolution

Language can evolve by means of natural

selection provided there were: (a) alternative

linguistic information-processing

mechanisms in ancestral populations; (b)

differences in linguistic information-

processing mechanisms were heritable; and

(c) some underlying linguistic information-

processing mechanisms conferred an

inclusive fitness advantage while others did

not.

Previous hypotheses

Group-benefit

• Gossip

• Social bonding

• Grooming

• Hunting

• Pair Bonds

Individual-benefit

• Motherese

• Sexual selection

• Song

• Mental toolkit

• Tool making

Számadó & Szathmáry (2006). Selective scenarios for the

emergence of natural language. Trends in Ecology and

Evolution, 21 (10), 555-561.

The fragility of cooperation

It is incorrect to assume that human

language must have evolved as a system of

harmonious cooperation. When cooperation

is observed it must be explained rather than

assumed (Brown, 2008).

Brown (2008). Sociogenomics for the cognitive adaptationist. In C.

Crawford & D. Krebs (Eds.), Foundations of evolutionary psychology

(pp. 171-182). Psychology Press/Lawrence Erlbaum.

Sender-receiver conflicts

“Language permits individuals to share

information and its use includes both signal

and receptor functions. Since other signal-

receptor systems seem susceptible to

super-stimulation (Ryan 1990), language

may provide an exceptional opportunity for

sensory exploitation…” (page 7)

Rice & Holland (1997). The enemies within: intergenomic

conflict, interlocus contest evolution (ICE), and the intraspecific Red

Queen Behavioral Ecology and Sociobiology, 41, 1-10.

Social transmission

Cultural systems must be susceptible to

sensory exploitation, as why else would we

have evolved cognitive mechanisms for

filtering out socially transmitted information?

Brown (2001). Genomic imprinting and the cognitive architecture

mediating human culture. Journal of Cognition and Culture, 1, 251-

258.

Intragenomic conflicts

“Perhaps the most interesting thing to come out of the realization of possible conflict

within the genome is a philosophical one. We see that we are not even in principle the

consistent wholes that some schools of philosophy would have us be.”

W.D. Hamilton FRS (1936-2000)

Parental investment (PI)

Defined as all care by a parent for offspring

that increases the likelihood that the

offspring survives at the expense of that

parents capacity to care for others (alive or

yet to be born). Examples of parental

investment include but are not limited to

gamete size, lactation, feeding, protection,

and teaching. Trivers R. (1972). Parental investment and sexual selection. In:

Campbell B, editor. Sexual selection and the descent of man 1871–

1971. Chicago: Aldine Press (p. 139–179).

Parent-offspring conflict

• Offspring are selected to extract more

resources than mothers are willing to give.

• Offspring are more closely related to

themselves than future siblings sired by

the same mother.

• In mammals with internal gestation,

multiple paternity and sex-biased dispersal

intragenomic conflicts within offspring are

expected.

Parental antagonism

Evolutionary theorist

David Haig has

hypothesised that

organisms are not

cohesive wholes and

conflicts between

parental genomes

within offspring are

expected.

Haig, D. (2000). Genomic imprinting, sex-biased dispersal, and

social behavior. Annals of the New York Academy of

Sciences, 907, 149–63.

Relatedness asymmetries

Barton, Surani, & Norris, M.L. (1984). Role of paternal and

maternal genomes in mouse development. Nature 311

(5984), 374–376.

What is genomic imprinting?

Keverne, Fundele, Narasimha, Barton, Surani (1996). Genomic

imprinting and the differential roles of parental genomes in brain

development. Developmental Brain Research, 92 (1), 91–100.

Parental antagonism theory

I suggest that language evolved for two

functions. First, as a means for offspring to

elicit resources from their parents (e.g. infant

crying as requests for food) benefiting

paternally-expressed genes. Secondly, to

fostering cooperation between maternal kin,

predicting that these cooperative functions

of language (e.g. infant cooing indicating

satiation), will be determined in part by

maternally-expressed genes.

Patrigenes Matrigenes

Tomasello, M. (2008). Origins of Human Communication. MIT Press.

Study One Questions

• What is the percentage of imprinted allelic

variants associated language phenotypes?

• Are these language-associated

phenotypes consistent with parental

antagonism theory?

• Prediction: The frequency of imprinted

genes involved in language phenotypes

will be greater than expected by chance.

Study One Methods

To test the hypothesis the Online Mendelian

Inheritance in Man (OMIM) database

(www.ncbi.nlm.nih.gov/omim ) was

consulted for allelic variants that have

effects on language (i.e., where the word

“language” was found in the full text search

of genes with and without allelic variants).

Study One Methods

Since chromosomal size could bias the

results, it was held constant in analyses by

dividing the frequency of language search

results by the estimated number of genes on

that chromosome. For example if language

loci were randomly distributed to each

chromosome, then we would expect the

likelihood of a „language‟ allele to occur on

the X chromosome would be approx seven

percent.

Study One Results

• Since only 1-2 percent of the mammalian

genome is imprinted we would not expect

any of the 14 „language loci‟ to be

imprinted unless parental antagonism had

played a role language evolution.

• Interestingly, 36 percent of language loci

uncovered in the OMIM database are

subject to possible parent-of-origin effects:

binomial test p < 0.001.

Study One Results

• The observed frequency of so-called

language loci on the X chromosome is 29

percent which is much higher than would

be expected by chance (binomial test p <

0.001).

• This unexpected finding is consistent with

the X-linked inhibitory bias hypothesis

(Haig, 2006), whereby relatedness

asymmetries could favour matrilineal

cooperative exchanges via language.

Angelman and

Prader-Willi Syndromes

• Sister genetic conditions with

critical epigenetic difference

(paternal or maternal mark).

• Angelman syndrome children

(pat > mat expression) are

good at making demands, but

never fully develop language.

Brown & Consedine (2004). Just how happy is the Happy

Puppet? An emotion signalling and kinship theory perspective

on the behavioral phenotype of children with Angelman

syndrome. Medical Hypotheses, 63, 377-385.

Communication

Transmission

Feuk et al. (2006) found that

the absence of paternal

FOXP2 gene among

individuals with Silver-

Russell Syndrome causes

developmental verbal

dyspraxia in the expressive

but not receptive domains.

Reception

Hamelin et al (2006) found

that Turner‟s syndrome

subjects with an X

chromosome of maternal

origin were less likely to

have sensorineural hearing

loss compared to those with

an X of paternal origin.

Human uniqueness?

• Overlapping genes are genes whose

transcription regions are shared.

Overlapping genes regulate key gene

expression mechanisms in genomic

imprinting.

• If imprinted genes played a special role in

the evolution of human language, we

expect to find significant differences

between chimpanzees and humans‟

overlapping imprinted loci.

Study Two Methods

• For investigating of evolutionary

relationships I used the Evolution

Visualizer for Overlapping Genes (EvOG)

http://neobio.cs.pusan.ac.kr/evog/

• It contains overlapping genes common

across Human, Chimpanzee, Cow,

Mouse, Chicken, Rat, Zebrafish etc.

Study Two Methods

Similarity of overlapping gene proximity.

Study Two Results

• Do human chromosomes with language

adaptations exhibit less similarity in their

overlapping imprinted genes compared to

chimpanzees?

• Seemingly not, as chromosome 11 has

significantly lower (both p‟s < 0.01)

similarity to chimpanzees (M = 0.89, SD =

0.14) than chromosomes 7 (M = 0.99,

SD = 0.01) and 15 (M =0.97, SD = 0.03):

[F (2, 157) = 23.22, p < 0.001].

Study Two Results

• Why Chromosome 11?

• The human-chimp divergence between

overlapping imprinted genes on

chromosome 11 is notable, because there

appears to have been recent natural

selection (Voight, Kudaravalli, Wen,

Pritchard, 2006), and chromosome 11

contains genes associated with

schizophrenia (Klar, 2004).

Study Two Results

• Interestingly, on chromosome 11 there has

been greater chimpanzee-human

evolutionary divergence in the maternally

expressed overlapping gene region H19,

OSBPL5 (similarity index = 0.5392)

compared to all other overlapping

imprinted gene pairs (mean similarity

index = 0.9471): t (174) = 57.86, p <

0.001. H19 is a growth suppressor gene.

t (100) = 3.41, p < 0.05

Levene‟s test

p < 0.001)

Study Two Summary

• Similarity between chimpanzees and

humans in overlapping imprinted genes

could either be due to constraint or

selection maintaining gene proximity.

• Divergence between human and

chimpanzee overlapping maternal genes

(compared to paternal gene pairs) is

consistent with Keverne‟s endocrinological

emancipation hypothesis.Keverne et al. (1996). Primate brain evolution: genetic and functional

considerations. Proc. R. Soc. Lond. B Biol. Sci. 263 (1371), 689–696.

Cultural Hitchhiking?

• If fissioning of parental language demes is

caused (in part) by conflicts within families,

then parentally- and maternally-biased

gene expression patterns could be

correlated with present-day language

diversity patterns.

• Hal Whitehead‟s (1998) idea of cultural

hitchhiking.

Whitehead, H. (1998). Cultural selection and genetic diversity in

matrilineal whales. Science, 282, 1708-1711.

Cultural Hitchhiking

‘Shibboleths’• Languages use arbitrary conventions to

signal meaning. This arbitrariness could

be a clue to origins. Signals restricted to

families of relatives, such as shibboleths

(i.e., signals only decodable by those who

are part of the group), probably are a key

characteristic of early hominin language

evolution.

• Can parental antagonism theory tell us

anything about language diversity?

How to test hypothesis

• One way to test this hypothesis is to have

information on a genetic element that

exhibits parent-of-origin effects, varies in

frequency across human populations with

differing levels of language diversity. An

example of „markers‟ that vary across

human populations are Alu elements

(note: one of my favourite „molecular

parasites‟)

Alu elements

• Alu elements are a family of

retrotransposons specific to primates

(often referred to as molecular fossils) that

were integrated early during primate

evolution.

• There are approximately 5000–7000 Alu

insertions unique to humans

Parent-of-origin Alu elements

• Imprinted genes and Alu insertion sites

share several characteristics

• One is that imprinted and Alu elements are

transcriptionally regulated by CpG

methylation.

• Another is that both imprinted and Alu

elements tend to cluster in the genome.

Waterland & Jirtle (2004). Early nutrition, epigenetic changes at

transposons and imprinted genes, and enhanced susceptibility to adult

chronic diseases. Nutrition, 20, 63-68

Parent-of-origin Alu’s

• Parent-of-origin effects have been found

among 19 Alu elements in a sample of 48

three-generation families.

• Six Alu polymorphisms were more strongly

methyated paternally relative to maternally

• Only one Alu element that exhibited

significantly stronger maternal methylation.

Sandovici et al. (2005). Interindividual variability and parent of origin

DNA methylation differences at specific human Alu elements. Human

Molecular Genetics, 14, 2135–2143

Study Three Methods

• I used the TranspoGene database,

(http://transpogene.tau.ac.il/) which

provides a complete Alu map of the

human genome, whereby each Alu

element is annotated with respect to

coding region and exon/intron location.

• Are Alu‟s inserting themselves in imprinted

language loci?

Alu’s and language loci

• As predicted, there was significantly higher

than expected frequency of Alu elements

inserted in the protein coding machinery of

imprinted language loci (472) versus the

number of Alu elements inserted into non-

imprinted autosomal language loci (124):

χ² (1) = 203.20, p < 0.001. A similar

pattern was revealed for the X-

chromosomal language loci.

Alu’s and language diversity?

• Language diversity was calculated using

Greenberg‟s index values from

www.ethnologue.com.

• Greenberg‟s language diversity index is

the probability that two randomly selected

people in a country would have different

first languages.

• Higher values (e.g., “1”) indicates that no

two individuals have the same first

language.

Study Three Methods

• To determine the language diversity for a

culture that resides across multiple

countries the mean index was used in

analyses.

• Larger cultural groups (i.e., African, Asian,

European, and Indian) were included as a

covariate in analyses to help reduce to

some extent the effects of shared

geographic region.

Study Three Results

• Controlling for larger cultural group, it was

found that the frequency of paternally-

silenced, but not maternally-silenced Alu

element insertions were positively

associated with language diversity across

cultures: partial r pat (28) = 0.54, p < 0.01;

partial r mat (28) = 0.35, p > 0.057.

• Alu elements exhibiting strongest

correlations with language diversity were

on Chromosome‟s 13 and 20.

Recap of Findings

• Theoretically I predict that paternal genes (within

the child) extract resources via demands on

mother; while maternal genes (within the child)

minimise demands via satiation cues.

• Imprinted and putatively imprinted genes (e.g.,

UBE3A & FOXP2) are implicated in language

phenotypes.

• Overlapping transcripts among maternal genes

(compared to paternal genes) show greater

evolutionary divergence.

Brown, W. M. (in press). The Parental antagonism theory of language evolution:

Preliminary evidence for the proposal. Human Biology

Recap of Findings

• So-called molecular parasites Alu

elements are likely to play an important

role in imprinted gene regulation of

language loci.

• Cultural hitchhiking of parentally-derived

Alu elements may track language

diversity.

What makes us human?(Eörs Szathmáry slide for “Darwin Day” at

the Collegium Budapest)

• Note the different time-scales involved

• Cultural transmission: language transmits

itself as well as other things

• A novel inheritance system

Conclusions

• Genomic imprinting plays a role in

language development and maternally-

derived overlapping transcripts show

greater evolutionary divergence.

• Cultures with more language diversity

appear to have more Alu paternal

silencing (relative to maternal silencing).

• Unlike previous approaches to language

evolution, parental antagonism is

inherently testable using genomic data.

Natural Sciences and Engineering Research

Council of Canada

David Haig, Ben Dickins, Lee Cronk;

Christopher Badcock, Bernie Crespi,

Alex Mesoudi, Pete Richerson , Boris Palameta;

Chris Moore; Harry Smit

Acknowledgments