Mitochondrial and nuclear discordance in a

widespread passerine: genomic

signatures of natural selection and local adaptation
Hernn E. Morales , Alexandra Pavlova , Leo Joseph , Richard Major , Nevil Amos , and Paul Sunnucks
1

hernan.morales@monash.edu

1Persistence and Adaptation Research Team, Monash University , Australia; 2Australian National Wildlife Collection, CSIRO, Australia;
3Australian Museum, Sydney, New South Wales 2010, Australia;

@HernMoral

Mitochondrial and nuclear structures are highly discordant

BACKGROUND: mitonuclear adapatation

Discordant patterns of mitochondria (mtDNA) and nuclear DNA (nDNA) genetic structure offer

Mitogroups

-15

-15

North
South

Inland
Coastal

great opportunities to study local adaptation (Toews and Brelsford, 2012)

Cell metabolic pathways (i.e. OXPHOS) depend on functional mitonuclear interactions and strong

Nuclear DNA

Maximum Temperature
> 33C

-20

selection is expected to maintain them (Dowling et al. 2008)

-20

28-33C
< 28C

Eastern yellow robin is a remarkable system for mitonuclear adaptation (Pavlova et al. 2013):

-25

-25

-30

-30

-35

-35

a) Two deeply divergent (~6.6%) mitochondrial groups (i.e. mitogroups): inland and coastal.
b) Distribution of mitogroups correlates with climatic variation after correcting for geography
c) Mitogroups overlap but mtDNA mixing is minimal, despite the absence of physical barriers
d) Nuclear genetic structure is minimal and perpendicular (i.e. discordant) to that of mtDNA
e) Sex-biased dispersal, vicariance or incomplete lineage sorting cannot explain the
divergence, so it is likely product of female-associated selection

140

Mitogenomes: positive selection against a

150

12000

count

100

8000

count

50

4000

0.2

0.6
Fst

0.4

0.8

0.6

1.0

0.8

Fst_NorthRegional

0.25Fst_NorthRegional
0.5
Fst

0.00

nDNA Inland / mtDNA Inland

1.0

0.25

0.75

0.50

0.75

Contact zone (40 Km radius)

nDNA Inland / mtDNA Coastal

COASTAL

Maximum Temperature

nDNA Coastal / mtDNA Inland

28-33C

nDNA Coastal / mtDNA Coastal

< 28C

* The maps are jittered for better visualisation, so sample location is approximate

Global Fst = 0.04

Transect 2

Outgroups

150

15000

count

100

10000

50

count

Sister species (Western Yellow Robin)

5000

* More details can be found in Morales et al. 2015; Molecular Ecology

0.2

0.4

0.2

0.6
Fst

0.4

0.8

0.6

1.0

0.8

Fst_SouthRegional

1.0

0.0

0.25Fst_SouthRegional
0.5
Fst

0.00

Summary

0.25

0.75

0.50

0.75

Genome-wide Fst at the contact zones

1RUWK/RFDO)VW/)00LQ*5((1&KU

1RUWK/RFDO)VW/)00LQ*5((1&KU

Transect 1

1.0

0.8

1RUWK/RFDO)VW/)00LQ*5((1&KU

1.0

North LocalFst LFMM in GREEN Unmapped

1RUWK/RFDO)VW/)00LQ*5((1&KU

1.0

Fst 99% quantile

1.0

1.0

Fst 90% quantile

0.8

0.8

0.8
Gene-environment
association (FDR, q=0.05)

0.8

0.4

0.2

6RXWK/RFDO)VW/)00LQ*5((1&KU

Transect 2
1

0.0

81.0 10

0.2

6RXWK/RFDO)VW/)00LQ*5((1&KU

11

12

13

14

15

17

18

20
1.0

21

22

23

24

25

26

27

Chromosome

0.6

0.8

Chromosome

10

0.4

0.6

1.0 7

0.4

0.2

0.0

11

12

13

14

15

Chromosome

17

18

19

20

21

22

23

24

25

26

27

0.8

0.4

0.6

0.4

0.2

0.2

0.0

0.0

Chromosome

1A

South LocalFst LFMM in GREEN Unmapped

10

12

28

Chromosome 1 position(Mb)

0.6

0.0

0.0

0.2

0.4

Chromosome

0.8

6RXWK/RFDO)VW/)00LQ*5((1&KU

28
1.0

0.2

0.0

Fst (W&C)

0.6

0.4

0.2

6RXWK/RFDO)VW/)00LQ*5((1&KU

0.0

19

Chromosome

Fst (W&C)

Fst (W&C)

FST

0.0

0.4

0.8

0.2

0.6

0.4

Chromosome

0.8

Fst (W&C)

0.6

Fst (W&C)

0.6

Fst (W&C)

0.6

Fst (W&C)

Fst (W&C)

Future directions

1.0

0.0

0.4

0.6

Fst (W&C)

Fst (W&C)

FST

0.2

References

0.4

0.2

0.0

N=18

Functionally annotate nuclear candidates for

selection
Are candidates disproportionately found in
OXOPHOS or sex-linked genes?
Analyse sex-specific patterns of genomic
differentiation
Is selection primarily impacting females?
Capture sequence of mitonuclear interactions
Link genomics to metabolic fitness

150

Photo: R. Clarke

Natural system with strong mitonuclear

discordance
Presumably product of local adaptation
Evidence of selection in mitochondrial
genomes
A small set of nuclear markers with the same
pattern

145

Global Fst = 0.026

Transect 1

INLAND

~6.6% divergence
61 fixed amino acid replacements
~98% coding region under
purifying selection
Evidence for 5 fixed amino acid
replacements under positive
selection

140

150

Local nuclear structure (> 45,000 SNPs)

background of strong purifying selection

N=14

145

1B 4A

Chromosome

LG2 0

4
6
8
10
Unmapped
markers

12

Chromosome 1 position(Mb)

SNPs position (chromosomes) mapped to Zebra Finch genome

D. K. Dowling, U. Friberg, J. Lindell, Evolutionary implications of non-neutral mitochondrial genetic variation. Trends in Ecology and Evolution 23, 546
(2008).
H. E. Morales, A. Pavlova, L. Joseph, P. Sunnucks, Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance.
Molecular Ecology 24, 2820 (2015)
A. Pavlova et al., Perched at the mitonuclear crossroads: divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear
gene flow in an australian bird. Evolution 67, 3412 (2013)
D. P. Toews, A. Brelsford, The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21, 3907 (2012).

Acknowledgments
I have received invaluable help from a lot of
people, including K. Delhey; B. Wang; J.
Bragg; A. Gonalves da Silva; R. Palmer; P.
Hanke; R. Clarke; D. Dowling and J. Wolff.
Thanks also to our funders.

Holsworth Wildlife Research Endowment

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