John Pannell Department 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)

Relative production of seeds or pollen (relative to hermaphrodites) Frequency of males or females Maintaining males versus females

Relative production of seeds or pollen (relative to hermaphrodites) Frequency of males or females Maintaining males versus females Gynodioecy under selfing & inbreeding depression

Relative production of seeds or pollen (relative to hermaphrodites) Frequency of males or females Maintaining males versus females Gynodioecy under selfing & inbreeding depression Androdioecy under 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 Male Steve Weeks

Several species of the Oleaceae Wallander, 2001

Durand (1963) Mercurialis annua

Established population males hermaphrodites Immigration males selected hermaphrodites selected with female-biased sex allocation Colonisation population growth reduced selfing

Obbard, Harris & Pannell (Am Nat, 2006) Within-population diversity Pair-wise differentiation

445 populations 5 transitions in breeding system 3 years of demographic sampling Males present Males absent

Males + females Hermaphrodites Dorken & Pannell (2007: Heredity)

Occupancy (% occupied sites) Abundance (number of plants) Males absent Males present Eppley & Pannell (2006: American Naturalist)

Dorken, Freckleton & Pannell (unpublished data) 25/171 49/185 Males present Males absent

2x Dioecy (West) Dioecy (Central) Dioecy (East) Monoecy Obbard, Harris & Pannell (American Naturalist, 2006) 6x

Dioecy (West) Dioecy (Central) Dioecy (East) Monoecy 6x Is there less inbreeding depression in northern populations of M. annua?

Pujol et al. (PNAS, 2009)

Dioecy (West) Dioecy (Central) Dioecy (East) Monoecy 6x Is there less quantitative genetic variation for sex allocation in northern populations of M. annua?

Pujol and Pannell (2008, Science)

hermaphrodites maleshermaphrodites Sex allocation Frequency

Male frequency Nutrient status

Dorken and Pannell (Current Biology, in press)

Durand (1963)

Korbecka and Pannell, unpubl. Selfing 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 + hermaphrodites 24–180 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

Male frequency Probability of finding a mate  = 0.9 = 0.9 = 0.1 (recessive load on W)  = 0.1 l = 0 (no recessive load on W)  = 0.9  = 0.5 l > 0 (recessive load on W) Maintenance of males

Male frequency Probability of finding a mate  = 0.9 = 0.9 = 0.1  = 0.1 l = 0 (no recessive load on W)  = 0.9  = 0.5 l > 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: Proc. Royal Soc., B (2004): 271: Evolution (2006)

father Male-sired seedlings grow 8% faster than hermaphrodite-sired seedlings Proc. Royal Soc., B (2004): 271: mother

Fraxinus ornus Hermaphrodites can be fathers but not grandfathers Hermaphrodites are functionally female Proc. Royal Soc., B (2004): 271: Evolution (2006)

Second puzzle… Females produce lots of pollen… Why? Fraxinus ornus F F M M Intense competition in the seed shadow

Second puzzle… Females produce lots of pollen… Why? Fraxinus ornus F F 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 NERC Royal Society BBSRC European Union