John PannellDepartment of Plant Sciences

University of Oxford

Possible links between sexual-system evolution and demographic processes in

plants and animals

Hermaphroditism

Gynodioecy

Androdioecy

(Male-sterility)

(Female-sterility)

0

0.1

0.2

0.3

0.4

0.5

0 2 4 6 8 10

Relative production of seeds or pollen(relative to hermaphrodites)

Fre

quen

cy o

f m

ales

or

fem

ales

Maintaining males versus females

0

0.1

0.2

0.3

0.4

0.5

0 2 4 6 8 10

Relative production of seeds or pollen(relative to hermaphrodites)

Fre

quen

cy o

f m

ales

or

fem

ales

Maintaining males versus females

Gynodioecyunder selfing & inbreeding depression

0

0.1

0.2

0.3

0.4

0.5

0 2 4 6 8 10

Relative production of seeds or pollen(relative to hermaphrodites)

Fre

quen

cy o

f m

ales

or

fem

ales

Maintaining males versus females

Gynodioecyunder selfing & inbreeding depression

Androdioecyunder selfing & inbreeding depression

Predictions

1. Androdioecy should be difficult to evolve

2. Androdioecy should occur only where hermaphrodites are prevented from selfing

In fact…

1. Androdioecy has evolved several times

2. Males typically occur with partially selfing hermaphrodites

Mercurialis annua Datisca glomerata Schizopepon bryoniaefolius

Occurrence of androdioecy

Kryptolebias marmoratus

Several species of branchiopod crustaceans

Sassaman, 1995

Herm

MaleSteve Weeks

Several species of the Oleaceae

Wallander, 2001

Durand (1963)

Mercurialis annua

Establishedpopulation

maleshermaphrodites

Immigration males selected

hermaphrodites selected with female-biased sex allocation

Colonisation

population growth reduced selfing

log(Geographic distance)

0.0 0.5 1.0 1.5 2.0 2.5

F' S

T/(

1-F' S

T)

0

1

2

3Hermaprodite populationsPopulations with males

Obbard, Harris & Pannell (Am Nat, 2006)

P < 0.001

0.11Males absent

0.43Males present

P < 0.001

0.11Males absent

0.43Males present

Within-population diversity

Pair-wise differentiation

• 445 populations• 5 transitions in breeding system• 3 years of demographic sampling

Males presentMales absent

Males + females

Hermaphrodites

Dorken & Pannell (2007: Heredity)

Occupancy (% occupied sites)

40 50 60 70 80 90 100

Abu

ndan

ce (

num

ber

of p

lant

s)

0

1000

2000

3000

4000

5000

6000

7000

Males absent

Males present

Eppley & Pannell (2006: American Naturalist)

Dorken, Freckleton & Pannell (unpublished data)

25/171

49/185

Males present Males absent

Longitude

-10 0 10 20 30

Alle

lic R

ich

ne

ss

1.0

1.1

1.2

1.3

1.4

1.5

1.6

1.7

1.8

2x

Dioecy (West)

Dioecy (Central)

Dioecy (East)

AndrodioeciousMonoeciousDioecious

Monoecy

Obbard, Harris & Pannell(American Naturalist, 2006)

Latitude

32 34 36 38 40 42 44

H' S

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

AndrodioeciousMonoecious

6x

Dioecy (West)

Dioecy (Central)

Dioecy (East)

AndrodioeciousMonoeciousDioecious

Monoecy

Latitude

32 34 36 38 40 42 44

H' S

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

AndrodioeciousMonoecious

6x

Is there less inbreeding depression in northern populations of M. annua? out

selfout

w

ww

Pujol et al. (PNAS, 2009)

Dioecy (West)

Dioecy (Central)

Dioecy (East)

AndrodioeciousMonoeciousDioecious

Monoecy

Latitude

32 34 36 38 40 42 44

H' S

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

AndrodioeciousMonoecious

6x

Is there less quantitative genetic variation for sex allocation in northern populations of M. annua?

Pujol and Pannell (2008, Science)

hermaphroditesmales hermaphrodites

Sex allocation

Fre

quen

cy

0.0 1.0

HIGH

LOW

HIGH

LOW

HIGH

LOW

6 Replicates

6 Replicates

6 Replicates

6 Replicates

Malefrequency

Nutrientstatus

Dorken and Pannell (Current Biology, in press)

Durand (1963)

Korbecka and Pannell, unpubl.

0.00

0.05

0.10

0.15

0.20

0.25

0.30

0.35

0.40

0.45

0.50

se

lfin

g r

ate

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

population

androdioecious patch monoecious patchSelfing rates in different patches

With males Without males

Dorken, Freckleton & Pannell (unpublished data) Eppley and Pannell (2008: Evolution)

Eulimnadia texana Datisca glomerata Schizopepon bryoniaefolius

Occurrence of males with hermaphrodites

Kryptolebias marmoratus

Herm

Male

Caenorhabditis elegans

Weeks et al. (2006)

Males + hermaphrodites24–180 million years ago Males + females

Hermaphrodites

Males and hermaphrodites in Eulimnadia species

Herm

Male

Why is androdioecy in Eulimnadia so ancient?

Hermaphrodites are the heterogametic sex

W/Z Z/Z

W/Z Z/Z

Deleterious recessives on W• NOT expressed• FIXED by drift

W/Z Z/Z

W/Z W/W

Selfing produces homozygous W• Load on W now expressed• Fitness of W/W < W/Z

Selection for reproductive assurance• Females produce an ovotestis• Androdioecy evolves

0

0.1

0.2

0.3

0.4

0.5

0.6

0 0.2 0.4 0.6 0.8 1

Mal

e fr

eque

ncy

Probability of finding a mate

= 0.9

= 0.9

= 0.1 (recessive load on W)

0

0.1

0.2

0.3

0.4

0.5

0.6

0 0.2 0.4 0.6 0.8 1

= 0.1

= 0(no recessive load on W)

= 0.9

= 0.5 > 0

(recessive load on W)

Maintenance of males

0

0.1

0.2

0.3

0.4

0.5

0.6

0 0.2 0.4 0.6 0.8 1

Mal

e fr

eque

ncy

Probability of finding a mate

= 0.9

= 0.9

= 0.1

0

0.1

0.2

0.3

0.4

0.5

0.6

0 0.2 0.4 0.6 0.8 1

= 0.1

= 0(no recessive load on W)

= 0.9

= 0.5 > 0

(recessive load on W)

Maintenance of males

Pannell (2008: Genetical Research)

Males maintained by overdominance?

• ZZ males: low fitness– can’t find a mate

• WW hermaphrodites: low fitness– reproductive assurance– BUT recessive genetic load on W chromosome

• WZ hermaphrodites: high fitness – reproductive assurance– AND sheltering of genetic load on W chromosome

Verdu, Montilla & Pannell (Proc. Royal Soc., B, 2004)

Fraxinus ornus

• Oleaceae family• Dioecy & androdioecy

are frequent in genus and family

First puzzle…

• Males and hermaphrodites co-occur

Fraxinus ornus

Implies androdioecy

• 1:1 sex ratio

Implies cryptic dioecy

• Hermaphrodites do sire seeds

Implies androdioecy

Functional Ecology (2002): 16: 858-869 Proc. Royal Soc., B (2004): 271: 2017-2023 Evolution (2006)

father father

Male-sired seedlings grow 8% faster thanhermaphrodite-sired seedlings

Proc. Royal Soc., B (2004): 271: 2017-2023

mothermother

Fraxinus ornus

Hermaphrodites can be fathers but not grandfathers

Hermaphrodites are functionally female

Proc. Royal Soc., B (2004): 271: 2017-2023 Evolution (2006)

Second puzzle…

• Females produce lots of pollen… Why?

Fraxinus ornus

FF

M

M

Intense competition in the seed shadow

Second puzzle…

• Females produce lots of pollen… Why?

Fraxinus ornus

FF

M

M

Intense competition in the seed shadow

Rival’s seedlings are less competitive

ESS: all females invest up to 50% of reproductive resources in pollen

Pannell (unpubl.)

Third puzzle…

• What is the mechanism of sabotage?

Thanks to…

• Darren Obbard• Richard Buggs• Stephen Harris• Sarah Eppley• Marcel Dorken• Paul Rymer• Rob Freckleton• Grazyna Korbecka• Stephen Weeks

• … and many undergraduate assistants

NERCRoyal SocietyBBSRCEuropean Union