The evolution and maintenance of plant sexual diversity

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• The evolution and maintenance of plant sexual
  diversity

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Why study polymorphic sexual systems?
Why is there high sexual diversity in flowering
plants?

• Immobility (rely on pollen vectors)
• Hermaphoditism (self-fertilization)
• Modular growth - get bigger by producing
  repeating organs via apical meristems
• (clonality and inter flower selfing)
• Closed carpel (mate selection e.g. SI)
• Life history diversity (mating patterns depend on
  longevity, plant size etc.)

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Outline

• Definitions and examples
• The evolution and function of stylar
  polymorphisms
• heterostyly
• enantiostyly
• flexistyly
• Major transitions
• The evolution of separate sexes from
  hermaphroditism (cosexuality)
• The evolution of self-fertilization from
  outcrossing (mating system evolution)

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sexual systems

• Sexual system the particular deployment of
  sexual structures within and among plants and the
  physiological mechanisms governing mating
• Sexual interference conflict in maternal and
  paternal functions resulting in gamete wastage
  and reduced fitness
• -physical interference, pollen clogging stigma,
  self fertilization etc
• -may or may not be associated with
  self-pollination

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Examples of plant sexual systems

• Dichogamy differences in the timing of pollen
  dispersal from anthers and stigma receptivity of
  flowers.

• protandry male phase comes before the female
  phase

• protogyny female phase comes before the male
  phase

Herkogamy the spatial separation of the anthers
and stigmas within a flower.
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mating systems
Mating system the mode of transmission of genes
from one generation to the next through sexual
reproduction (e.g. maternal selfing rate)
Selfing rate (s) the proportion of seeds that
are self fertilized Outcrossing rate (t1-s)
the proportion of seeds that are
outcrossed Inbreeding depression the reduction
in viability and fertility of inbred offspring
compared with outbred offspring. ?1-ws/wo
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Inbreeding depression in Collinsia verna

• Mean inbreeding depression ?0.15
• Low relative to many outcrossing plants

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Homomorphic self incompatibility
Two main types of homomorphic incompatibility (up
to 50 angiosperms)
-gametophytic incompatibility phenotype is
determined by its haploid genotype e.g. S1 or S2
can not fertilize S1 S2 plants but S3 pollen
can -sporophytic incompatibility governed by
the genotype of the pollen producing parent e.g.
any pollen from and S1S2 plant can not fertilize
an S1_ or S2_ plant
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polymorphic sexual systems

• The co-occurrence within a population of
  morphologically distinct mating groups
  distinguished by differences in their sexual
  organs

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Why study polymorphic sexual systems?
Why study plant polymorphic sexual systems?

• simple inheritance
• sexual morphs easily identified in the field
• under strong frequency-dependent selection
• theoretical models provide predictions
• manipulative experiments possible

Sagittaria latifolia
Cyanella alba
Long-styled
Short-styled

• Primula polyneura

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Floral design and pollen transfer heterostyly
Heterostyly two (distyly) or three (tristyly)
style morphs differ in the reciprocal placement
of anthers and stigmas.

• reciprocal sex-organ placement
• heteromorphic
• self-incompatibility
• (disassortative mating)
• genetic polymorphism

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Floral design and pollen transfer
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Pollen transfer and equilibrium morph ratios in
typical tristyly
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Pollen transfer and equilibrium morph ratios in
typical tristyly
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Pollen transfer and equilibrium morph ratios in
typical tristyly
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Pollen transfer and equilibrium morph ratios in
typical tristyly
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Equilibrium morph frequencies

• Disassortative mating results in negative
  frequency-dependent selection
• Equal morph ratios are predicted
• 111 found in many tristylous populations

R.A. Fisher
Lythrum salicaria
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Floral design and pollen transfer enantiostyly
Enantiostyly mirror image flowers in which the
style bends either to the left or the right side
of the floral axis-deposits pollen on the left or
right side of the bee.
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Floral design and pollen transfer

• Created straight styled, monomorphic and
  dimorphic arrays from Solanum rostratum
  (monomorphic)
• Highest outcrossing rate in dimorphic arrays
• Most of the mating was intermorph in the
  dimorphic array
• (negative frequency dependent selection)

Jesson and Barrett 2002 Nature
Inter-morph mating
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Floral design and pollen transfer

• Herkogamy reduces self pollination (and other
  forms of sexual interference)
• Separation reduces precision of cross pollination
  (lower male and female fitness-pollen wastage and
  pollen limitation)
• Reciprocal herkogamy improves pollen transfer
  efficiency
• Polymorphisms is generally maintained by
  disassortative mating at equal frequency

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Flexistyly

• Flexistyly populations contain two floral morphs
  that differ in there temporal patterns of style
  growth and orientation

Alpinia

• combines herkogamy and dichogamy
• found in tropical gingers

protandrous protogynous
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The evolution of separate sexes

• Gender is the relative contributions that plants
  make to the next generation as a male and female
  parent (quantitative measure)

• Monomorphism - continuous variation in gender
• Dimorphism - two distinct sexual morphs that
  function primarily as a male or female parent

Dioecy Gynodioecy Androdioecy
Sagittaria latifolia
Mercurialis annua
Silene vulgaris
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Evolutionary pathways to gender dimorphism

• Gynodioecy pathway
• Monoecy pathway
• Distyly pathway
• Heterodichogamy pathway

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Selective mechanisms and the evolution of
separate sexes
The evolution of dioecy from gynodioecy Nuclear
inheritance of male sterility (female)

• Females spread if they produce at least two
  times as many seeds as hermaphrodites
• s ? gt 0.5 (more than half the offspring of
  hermaphrodites die due to inbreeding depression)
• -resource reallocation from male function to
  female function (females produce gt2x as many
  ovules)

w for invasion Pollen 1
0 Seed 1 gt2
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Cyto-nuclear control of gender dimorphism
Sterility mutations can occur in the maternally
inherited mitochondrial genome All offspring of
the male sterile mutant with be female Females
can spread with only a slight female fertility
advantage
Dioecy can then evolve from gynodioecy as
hermaphrodites invest in male function
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Selective mechanisms and the evolution of
separate sexes

• Lycium - self incompatibility lost with
  chromosome doubling
• Polyploids are gender dimorphic (independent
  evolution in NA and south Africa)
• Association between polyploidy and dimorphism
  also found in 12 unrelated genera in other
  families

Miller and Venable 2000
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Selective mechanisms and the evolution of
separate sexes

• Large plant size (e.g. clonal)-gthigher selfing
  rates
• Geitonogamy (transfer of self pollen between
  flowers)

Sagittaria latifolia Dioecious large
clones Monecious (hermaphrodites) smaller
plants s ? gt 0.5 in some monecious populations
Dorken et al 2002
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Selective mechanisms

• Resource allocation
• resource poor environments hermaphrodites
• unable to maintain both sex functions
• e.g. Wurmbea dioica
• gynodioecy in good environments
• dioecy in poor environments

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Evolutionary transitions from outcrossing to
selfing
Amsinckia
outcrosser selfer

• Multiple origins of self-fertilization
• Morphological changes in flower size accompany
  self-fertilization

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The evolution of self-fertilization

• 20 of angiosperms species have evolved a
  predominantly selfing strategy
• costs of selfing
• inbreeding depression

• Why do so many species self despite the costs?

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Self fertilization
Benefits of selfing i. Transmission advantage
(Fisher) pollen parent seed parent
total outcrossing 1 1 2 selfing (1
out1self2) 1 3 ii. Reproductive assurance
assured reproduction through selfing when
conditions for outcrossing are not favourable
(absence of mate or pollinators)
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Selfing rate and pollination failure in
Collinsia verna

• Selfing rates varied between years and
  populations (context dependent)
• Correlated with pollination failure indicating
  reproductive assurance

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Self fertilization

• Costs of selfing
• Inbreeding depression-transmission advantage lost
  if ? gt 0.5
• ii. pollen discounting the loss in outcrossed
  siring success as a result of self-pollination
• iii. seed discounting the formation of
  self-fertilized seeds from ovules that, if they
  had not been self-fertilized would have been
  cross-fertilized

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Pollen discounting in Eichhornia paniculata
Harder and Barrett 1995 Nature
Negative relations between outcrossed siring
success and selfing rate provides evidence for
pollen discounting
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Seed discounting in Aquilegia canadensis
Test of reproductive assurance hypothesis Emascul
ations reduce seed set by 14 Reduced selfing by
40 High inbreeding depression, seed discounting
costly
Herlihy and Eckert 2002 Nature
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The evolution of self-fertilization
Theory predicts either the evolution of selfing
or outcrossing but many species have a mixed
mating strategy