Population size does not influence mitochondrial genetic diversity in animals

E. Bazin, S. Glémin, N. Galtier

CNRS UMR 5171 – Génome, Populations, Interactions, AdaptationUniversité Montpellier 2

Montpellier, France

galtier@univ-montp2.fr

DAWG meeting 2006

Evolutionary forces influencing the genetic diversity

~ Ne .

selection

demography

structure

mating systems

On average, abundant species should be more polymorphic than scarce ones.

Allozyme meta-analyses

- Hamrick & Godt 1996 : outcrossers > selfers (plants)

- Nevo et al 1984: invertebrates > vertebrates (animals)

- Frankham 1997: mainland > island (animals and plants)

- Spielman et al 2004: healthy > endangered (animals and plants)

What about DNA markers, especially mtDNA?

The Polymorphix data base

GenBank/EMBL

species 1

BLAST

similarity

CLEAN

bibliographyflanking

ALIGN

Polymorphix families

ADDOUTGROUPS

http://pbil.univ-lyon1.fr/~polymorphix

Measuring DNA polymorphism in animals

- remove genome projects

- remove transposons, LINE, SINE, MHC, immunoglobulin, rRNA …

- manually check highly polymorphic families

- start from Polymorphix 1.2 - Metazoa

- focus on coding sequences

- for each family, calculate the synonymous diversity s

- average over loci within species

- average over species within 8 taxa: Mammals, Sauropsids, Amphibians, Fish

Insects, Crustaceans, Molluscs, Echinoderms

- compare to allozyme data (Nevo et al 1984)

Mammals

Sauropsids

Amphibians

Fish

Insects

Crustaceans

Molluscs

Echinoderms

311

348

80

248

26

451

58

107

25

18

4

11

22

69

2

11

184

116

61

183

15

122

122

46

mtDNA nuclear DNA allozymes

1629 162 849

Data set: number of species

Taxonomy does not predict mtDNA sequence polymorphism

s

Allozyme heterozygosity

nuclear DNA

Verterbates Inverterbates

Taxonomy does not predict mtDNA sequence polymorphism

s

Allozyme heterozygosity

nuclear DNA

mtDNA

Verterbates Inverterbates

Ecology does not predict mtDNA sequence polymorphism

Crustaceans

Branch. Dec. Branch. Dec.

0.10

s

0.30

H

Allozymes mtDNA

**

Ecology does not predict mtDNA sequence polymorphism

Crustaceans

Branch. Dec. Branch. Dec.

0.10

s

0.30

H

Allozymes mtDNA mtDNAAllozymes

0.400.08

sH

continent marine continent marine

Molluscs

** *

Ecology does not predict mtDNA sequence polymorphism

Crustaceans

Branch. Dec. Branch. Dec.

0.10

s

0.30

H

Allozymes mtDNA mtDNAAllozymes

0.400.08

sH

continent marine continent marine

Molluscs

mtDNAAllozymes

Fish

H s

0.08 0.08

fresh marine fresh marine

** *

*

Ecology does not predict mtDNA sequence polymorphism

Crustaceans

Branch. Dec. Branch. Dec.

0.10

s

0.30

H

Allozymes mtDNA mtDNAAllozymes

0.400.08

sH

continent marine continent marine

Molluscs

mtDNAAllozymes

Fish

H s

0.08 0.08

fresh marine fresh marine

** *

*

mtDNAdiversity

mass (log scale) mass (log scale)

taxonomyresidual

Ecology does not predict mtDNA sequence polymorphism

Mammals

r2 : 3%p-val : 0.04

r2 : 0.1%p-val : 0.6

Why is not mtDNA sequence polymorphism correlated to Ne?

- mutation: would imply a general, unplausible inverse relationship between Ne and

- demography, structure: should affect the nuclear genome as well

- natural selection:

. negative selection = background selection: still predicts a positive relationship between and Ne (Charlesworth et al 1995)

. positive selection = genetic draft predicts an essentially flat relationship between and Ne (Gillespie 2001)

Selective sweep, hitch-hiking and genetic draft

SELECTIVE SWEEP

sampled neutral locus

linked selected locus

A selective sweep, the rapid fixation of an advantageous mutation leads to sudden drop of variability at linked loci through hitch-hiking.

Advantageous mutations are more frequent in large populations:the increased genetic draft compensates for the decreased genetic drift.

Selective sweep, hitch-hiking and genetic draft

A selective sweep, the rapid fixation of an advantageous mutation leads to sudden drop of variability at linked loci through hitch-hiking.

Advantageous mutations are more frequent in large populations:the increased genetic draft compensates for the decreased genetic drift.

Ne

drift draft

Synonymous / non-synonymous evolutionary process

- Neutrality Index: NI = (N / S) / (dN / dS)

Vert. Invert. Vert. Invert.

mtDNA nuclear DNA

0

1

5

10

NI (log scale)

**adaptative

purifying

neutral

Synonymous / non-synonymous evolutionary process

- Neutrality Index: NI = (N / S) / (dN / dS)

Vert. Invert. Vert. Invert.

mtDNA nuclear DNA

0

1

5

10

NI (log scale)

**adaptative

purifying

neutral

Synonymous / non-synonymous evolutionary process

- Neutrality index: NI = (N / S) / (dN / dS)

Vert. Invert. Vert. Invert.

mtDNA nuclear DNA

0

1

5

10

NI (log scale)

adaptive

purifying

neutral

Synonymous / non-synonymous evolutionary process

- complete mitochondrial genome:

data sets average dN/dS

Vertebrates

Invertebrates

88 0.086

24 0.151**

Conclusions

- population size influences nuclear, but not mitochondrial DNA diversity

- recurrent adaptive evolution explains the homogeneous mtDNA pattern

Implications

- low-diversity mtDNA lineages might be well adapted, not endangered

- mtDNA might be the worst marker of species abundance

Questions

- what is mtDNA adapting to ?

- mtDNA might be a good marker for barcoding