Diversity of plant mating systems and their evolutionary consequences

Question 1

The evolution of sexual reproduction

Answer 1

Sexual reproduction is a fundamental cornerstone of evolutionary biology

The costs of finding a mate are outweighed by the benefits of recombination generating new genetic combinations allowing sharing of beneficial mutations and purging of deleterious ones.

Question 2

Sexual reproduction and complexity

Answer 2

Sexual reproduction predominates in eukaryotes in contrast to prokaryotes suggesting a link between complexity and sexual reproduction.

Complexity
- more genes
- larger genomes
- mitochondria and chloroplasts
+ (intracellular ROS can cause mutations)

Sexual Reproduction
- recombination
- deleterious mutations repaired
- adaptive mutations spread
- new genetic combinations

Question 3

Sexual reproduction in higher plants

Answer 3

Higher plants with an extended sporophyte stage have developed increasingly complex adaptations for sexual reproduction.

Higher plants still need to find a suitable mate despite the constraints of being immobile terrestrial organisms.

In an algae , all tissue perform all tasks
whereas in higher plants leaves, stems and roots (and the various cells within them) perform specific roles

Question 4

Selfing mating systems

Answer 4

In contrast to most animals, plants show highly diverse reproductive strategies to overcome being sessile organisms that cannot physically move to find a compatible mate

Very broadly, reproductive strategies can be classified as inbreeding, where an individual is sufficient for reproduction, or outcrossing, where a compatible mate is required

Many plants are potentially capable of inbreeding by selfing because they have hermaphrodite flowers with male and female reproductive organs in the same flower

Question 5

Outcrossing mating systems

Answer 5

Plants achieve outcrossing via a diversity of outcrossing mechanisms and their reproductive structures show many adaptations to promote efficient cross-pollination

Question 6

Outcrossing breeding systems: Anemophilous (wind pollinated)

Answer 6

Anemophilous, wind pollinated species, have exposed structures often without petals, produce lots of small pollen, and have large sticky stigmas

“Many of the world’s most important crop plants are wind-pollinated. These include wheat, rice, corn, rye, barley, and oats. Many economically important trees are also wind-pollinated. These include pines, spruces, firs and many hardwood trees, including several species cultivated for nut production. “
https://seeds.ca/pollinator/bestpractices/wind_pollination.html

Question 7

Outcrossing breeding systems: Entomophilous (insect pollinated) and Zoophilous (bird or mammal pollinated)

Answer 7

Entomophilous, insect pollinated species, have showy petals, scent and nectar glands, nutritious pollen, and precise arrangement of reproductive organs.

Zoophilous, bird or mammal pollinated species, have specific adaptations to attract their specialized pollinators

Question 8

Dichogamy

Answer 8

flowers with dichogamy express different aspects at different stages of maturity

Flowers commonly show temporal separation of reproductive development to prevent self-pollination

Protogyny: stigmas become receptive before anthers shed pollen

Protandry: anthers shed pollen before stigmas become receptive

Question 9

Herkogamy

Answer 9

Outcrossing can be promoted by herkogamy, physical separation of the male and female reproductive organs, to prevent self-pollination within the same flower

Many flowers show herkogamy that can change as the flower develops

Question 10

Heterostyly

Answer 10

Heterostyly is a form of herkogamy where two or more distinct flower structures have evolved

to promote cross-pollination

Example: Pin and thrum flower morphs of primrose

Outcorssing by heterostyly
Distinct flower forms in the same species that promote pollen transfer between forms

Question 11

Monoecy and dioecy

Answer 11

some species have male and female plants e.g. Holly and this ensures outcrossing

Separate male and female flowers either on the same plant (monoecy: maize, squash) or different plants (dioecy: datepalm, fig, kiwi)

Dioecious plants are obligately outcrossing but at a cost of male individuals being unable to produce seed.

This cost is offset by males’ potential ability to pollinate many females.

Question 12

Sex determination

Answer 12

Entire chromosomes devoted to sex determination represent the greatest genomic change in response to selection for outcrossing.

Plants are useful for the study of sex determination as they have repeatedly evolved breeding systems based on separate sexes (dioecy) from hermaphrodite progenitors.

Related species show intermediate evolutionary steps from hermaphrodites to dioecy determined by sex chromosomes.

Pannell (2017) Current Biology 27: R191

Question 13

Self-incompatibility

Answer 13

Self-incompatibility (SI) is a common genetic mechanism to prevent self-fertilization found in over 100 plant families and 39% of angiosperms overall

The female reproductive tissues can recognize and reject self and related pollen

Controlled by single genetic locus which is known as a supergene, S, coding for pollen ligands and their specific stigma/style receptors

Some important crop species show SI (apple, brassica, cacao, ryegrass)

Question 14

Self-incompatibility alleles

Answer 14

Self-incompatibility has independently evolved several times but its underlying function is a convergent “lock and key” mechanism.

In the case of selfing, the male gametes release specific signalling molecules that bind to female expressed receptors activating a gamete rejection signalling pathway.

In the case of outcrossing, the male ligands are not recognized by the female receptors from a different individual and the fertilization interaction proceeds.

Question 15

The S Locus

Answer 15

Female SI receptors only recognize “self” male ligands and do not interact with other alleles of male ligand.

Each pair of interacting receptors and ligands need to be inherited together as a unit to maintain self-incompatibility. This is achieved by linking them physically into an S locus, also known as an S supergene or haplotype.

Pairs of interacting male and female determinants are kept together by inhibiting recombination in this genomic region.

Highly reordered S haplotypes contribute to limiting recombination.

Question 16

Types of self-incompatibility: Gametophytic

Answer 16

Male expression is under control of male gametophyte – haploid so only one expressed in male and two in female

Pollinations involving the same S allele trigger a pollen rejection response to prevent self-fertilization

In gametophytic SI (GSI), each haploid pollen expresses its own single S allele.

Half-compatible cross outcomes are possible where individuals share one S allele (e.g. siblings, centre image)

Question 17

Types of self-incompatibility: sporophytic

Answer 17

In sporophytic SI (SSI), both male S proteins of the diploid paternal parent are deposited in the pollen coat during pollen development.

This provides more effective control of crosses between related individuals

Question 18

Molecular genetic control of GSI

Answer 18

The molecular genetic basis of two forms of GSI are known in Papaveraceae (left) and Rosaceae (right, this system is shared with several other plant families)
mobile element is female gene, activated by lock and key

Question 19

Molecular genetic control of SSI

Answer 19

The molecular genetic basis of one form of SSI is known in Brassicaceae.

In all types of SI, the molecular basis of SI shares similarities with pathogen defence from which it probably evolved.

see notes for diagram

Question 20

Evolution of new S alleles

Answer 20

New S alleles evolve rarely at a slow rate because at least two mutations in each of the male and female expressed genes are required.

The two new mutations need to be complementary so that a new specific ligand-receptor pair is generated.

Intermediate steps are self-compatible and therefore unfit.

Question 21

Selection at the S locus

Answer 21

The S locus experiences a form of balancing selection called negative frequency-dependent selection.

Rare or new S alleles have the advantage of relatively greater mate availability in terms of the proportion of compatible mates in a population.

The same process tends to equalize S allele frequencies within populations

Rarer alleles have a greater proportion of compatible mates

Question 22

S locus diversity

Answer 22

Despite the slow rate of origin of new S alleles, negative frequency dependent selection (NFDS) typically leads to the accumulation of high S allele diversity (10 – 200! alleles per species)

NFDS promotes the spread and sharing of S alleles between populations and even species.

NFDS maintains S alleles through long periods of evolutionary time.

Castric & Vekemans (2004) Mol. Ecol. 13: 2873

Lawrence (2000) Ann. Bot. 85: 221-226

Question 23

S locus evolution

Answer 23

Strong negative frequency dependent selection contributes to the maintenance of S alleles over long evolutionary periods, often predating speciation.

see diagram in notes: In the example S allele phylogenetic tree, there are many pairs of closely related S alleles between two SI Arabidopsis species (A. lyrata in blue, A. halleri in red) suggesting these alleles predate speciation. There are even some S alleles more closely shared with a different genus (Brassica oleraceae in green)

Question 24

examples in nature

Answer 24

Ragwort hybridisation Mt etna
Senecio squalidus introduction to UK

Question 25

Controlled crossing studies of SI

Answer 25

The molecular genetics of SSI is not yet known in Asteraceae but when the genes controlling SI are not known, S alleles can still identified by observing the outcomes of controlled crosses.

Individuals that are incompatible with each other share S alleles.

Completing all the paired-cross combinations in a sample allows all S alleles to be identified.

Question 26

Controlled crossing studies of SI example

Answer 26

Brennan et al 2002
Controlled in-vivo self- and cross-pollinations
No seeds produced when parents share expressed S alleles
Analysis of paired cross combinations between sample individuals to identify S alleles and dominance interactions

Crossing studies of Sicilian Senecio taxa
- Crosses were performed for population samples of
S. aethnensis
- both species and their hybrids showing widespread S allele sharing between species.
- Negative frequency dependent selection promotes the spread of S alleles

(Brennan et al. (2013) Evolution 67: 1347)

Question 27

Mating system shifts

Answer 27

Plants sometimes undergo mating system shifts and the most typical change is from outcrossing to inbreeding.

The relative balance between the advantages of outcrossing and the advantages of inbreeding alters to favour inbreeding.

Question 28

Climate change and anthropogenic changes are leading to widespread declines in pollinator abundance. Many flowering plants are evolving as a result, but outcomes can be difficult to predict.

Answer 28

examples:

Morning glory (Ipomoea purpurea) invested more in floral display over a period from 2003 to 2012 to attept to ensure more visits from pollinators
(Bishop et al. 2023 Evol. Lett. 7:88)

Field pansy (Viola arvensis) invested less in floral display and increased selfing rates by 27% over a period from 2000 to 2021 investing more energy in selfing due to a reduction in pollinators (Acoca-Pidolle et al. 2023 New Phytol. doi: 10.1111/nph.19422

Question 29

Benefits of outcrossing

Answer 29

Some of the advantages of outcrossing have been covered previously:

new genetic combinations

recombination that allows sharing of beneficial mutations and purging of deleterious mutations

These are medium term advantages but only short term advantages can be selected. The most important short term advantages are:

Within-individual genetic variation (heterozygosity)

Masking of genetic load (avoidance of inbreeding depression)

Question 30

Outcrossing and genetic diversity example

Answer 30

C. grandiflora and C. rubella
outcrosser has more variation than the selfer
(Foxe et al 2009)

Question 31

Selfing and genetic diversity

Answer 31

Repeated generations of selfing lead to a rapid loss of heterozygosity within individuals

Selfing is a extreme form of inbreeding where the chance that the pair of genes at each locus is the same because of common descent (Inbreeding coefficient, F) increases by 50 % per generation

Example of progeny genotypes resulting from a heterozygous selfing: every time you self 50% are homozygous

Question 32

Selfing and approach to homozygosity

Answer 32

Inbreeding leads to a rapid approach to homozygosity within individuals a just a few generations

Question 33

Inbreeding depression

Answer 33

Mutation generates a genetic load of alleles with deleterious effects but these effects can often be compensated by the non-mutated complementary allele in heterozygous state.

Selfing exposes these deleterious alleles and their effects as homozygotes leading to reductions in fitness known as inbreeding depression.

However, expressed deleterious alleles makes selection more efficient at removing them and reducing the genetic load.

Therefore, selfing causes expression of inbreeding depression but also allows for inbreeding depression to be selectively removed over time.

Question 34

Benefits of selfing:

Answer 34

The major benefits of selfing are reproductive assurance
and the ability to spread under conditions that threaten mate availability.

Many ecological factors can limit MA and RA including:
-small population size
-low density
-range margin
-population fragmentation
-Colonization
- disturbance
- stress
- limited pollination

Question 35

Evolutionary consequences of
mating system shifts

Answer 35

• Species can show shifts in mating system over time. The shift from outcrossing to selfing is more common than the opposite
• Mating system shifts can be associated With diversification and situation such as when some but not all populations of an outcrosser become selfing
  -Diversification in outcrossers is driven by sexual and genomic conflicts while in selfers it is driven by isolation.
• Extinction in outcrossers is driven by lack of potential mates while in selfers it is driven by lack of mutations and lack of adaptive potential
  Wright al. (2013) Proc RSoc a 280: 20130133

Question 36

Evolutionary comparisons

Answer 36

Analyses of the phylogenetic distributions of mating systems
indicate that selfers tend to have shorter branches.
In other words, selfers turnover (speciate and extinguish) more rapidly than outcrossers.

Goldberg et al (2010) Science 330: 493

Question 37

Lecture summary

Answer 37

Sexual reproduction promotes greater organismal complexity alongside other evolutionary advantages.

Plants have evolved many adaptations to facilitate sexual reproduction in response to the challenges of being sessile terrestrial organisms.

Many plants have hermaphrodite reproductive structures and are capable of either selfing or outcrossing.

Outcrossing mechanisms can be physical adaptions such as dichogamy, herkogamy, or dioecy or molecular mechanisms such as self-incompatibility.

Self-incompatibility is an innate self-pollen recognition and rejection mechanism that has convergently evolved many times across flowering plants.

Two major forms of SI different in their mode of pollen expression and the genes responsible.

The S locus experiences strong negative frequency dependent selection that generates high polymorphism over evolutionary time.

SI influences plant demographics and evolution.

Mating system shifts from outcrossing to inbreeding regularly occur in plants if the relative advantages of either mode of reproduction change.

Short term benefits of outcrossing are related to greater within-individual genetic diversity, while short term benefits of selfing are related to mate availability and reproductive assurance.

Mating system variation affects evolutionary processes and has macroevolutionary consequences on speciation and extinction rates.