Possible links between sexualsystem evolution and demographic processes

Possible links between sexual-system evolution and demographic processes in plants and animals John Pannell Department of Plant Sciences University of Oxford

(Male-sterility) Gynodioecy Hermaphroditism Androdioecy (Female-sterility)

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

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

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

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

Occurrence of androdioecy Mercurialis annua Kryptolebias marmoratus Datisca glomerata Schizopepon bryoniaefolius

Several species of branchiopod crustaceans Herm Sassaman, 1995 Male Steve Weeks

Several species of the Oleaceae Wallander, 2001

Mercurialis annua Durand (1963)

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

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

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

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

Abundance (number of plants) 7000 Males present 6000 5000 4000 3000 Males absent 2000 1000 0 40 50 60 70 80 90 100 Occupancy (% occupied sites) Eppley & Pannell (2006: American Naturalist)

49/185 25/171 Males present Males absent Dorken, Freckleton & Pannell (unpublished data)

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

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

Pujol et al. (PNAS, 2009)

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

Pujol and Pannell (2008, Science)

hermaphrodites Frequency males 0. 0 Sex allocation 1. 0

Male frequency Nutrient status

Dorken and Pannell (Current Biology, in press)

Durand (1963)

Selfing rates in different patches With males Without males Korbecka and Pannell, unpubl.

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

Occurrence of males with hermaphrodites Eulimnadia texana Datisca glomerata Schizopepon bryoniaefolius Herm Male Kryptolebias marmoratus Caenorhabditis elegans

Herm Males and hermaphrodites in Eulimnadia species Male Hermaphrodites Weeks et al. (2006) Males + hermaphrodites 24– 180 million years ago Males + females

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 Selection for reproductive assurance • Females produce an ovotestis • Androdioecy evolves W/Z Z/Z W/W Selfing produces homozygous W • Load on W now expressed • Fitness of W/W < W/Z

Maintenance of males 0. 9 ==0. 9 Male frequency = 0. 1 = 0. 9 =0 (no recessive load on W) = 0. 5 >0 (recessive load on W) = 0. 1 (recessive load on W) Probability of finding a mate

Maintenance of males 0. 9 ==0. 9 Male frequency = 0. 1 = 0. 9 =0 (no recessive load on W) = 0. 5 >0 (recessive load on W) = 0. 1 Probability of finding a mate 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

Fraxinus ornus • Oleaceae family • Dioecy & androdioecy are frequent in genus and family Verdu, Montilla & Pannell (Proc. Royal Soc. , B, 2004)

First puzzle… • Males and hermaphrodites co-occur Implies androdioecy • 1: 1 sex ratio Implies cryptic dioecy • Hermaphrodites do sire seeds Implies androdioecy Functional Ecology (2002): 16: 858 -869 Fraxinus ornus Proc. Royal Soc. , B (2004): 271: 2017 -2023 Evolution (2006)

father mother Male-sired seedlings grow 8% faster than hermaphrodite-sired seedlings Proc. Royal Soc. , B (2004): 271: 2017 -2023

Hermaphrodites can be fathers but not grandfathers Hermaphrodites are functionally female Fraxinus ornus Proc. Royal Soc. , B (2004): 271: 2017 -2023 Evolution (2006)

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

Second puzzle… • Females produce lots of pollen… Why? M F F Rival’s seedlings are less competitive M ESS: all females invest up to 50% of reproductive resources in pollen Intense competition in the seed shadow Fraxinus ornus 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