Plant Speciation

1
Plant Speciation Evolution (PBIO 475/575)

• Hybridization

2
General Principles

• Hybridization sensu lato cross-fertilization
  that brings two different genotypes into
  conjunction
• May involve different individuals within a
  population or individuals among populations
  ("trivial") or
• individuals of different taxa (e.g., distinct
  species--usually what people mean by
  hybridization)
• May be restricted to the initial hybridization
  event, or it may continue through time and across
  generations where weak isolation mechanisms
  permit gene flow between original parents and
  hybrid progeny

3
General Principles

• Previously believed to be unimportantan
  evolutionary dead end
• Much new evidence demonstrates that hybridization
  provides new genetic combinations available for
  modification by other processes e.g.,
  polyploidy, chromosomal rearrangements, selection
  on introgressants
• Often disrupts isolation mechanisms preventing
  interspecific gene flow if it occurs over wide
  geographic areas and impacts many populations of
  hybridizing species ? genetic swamping

4
General Principles

• In groups where hybridization is common, it is
  involved in formation of new geographic and
  ecological races
• e.g., Redroot (Ceanothus)

Raven et al. (1992)
5
General Principles

• Hybrids not commonly "perfectly" intermediate in
  phenotype
• Hybrid vigor commonly expressed, especially in
  F1s
• Different traits often vary toward one of the
  parental taxa
• Sometimes a novel expression arises
• e.g., unique non-glandular hair type in hybrid
  false foxglove, Aureolaria flava x pedicularis
• e.g., dense glands of hybrid woodsia fern,
  Woodsia ilvensis x oregana, that are not found in
  the parent species

6
General Principles

• Hybrids may be exceedingly localized or rare, or
  geographically very widespread, depending on
  frequency of hybridization event
• e.g., exceedingly rare hybrid cinnamon fern,
  Osmunda x ruggii
• known historically from one plant in each of two
  widely separate sites in the eastern U.S.
• parents grow sympatrically over thousands of
  square miles
• only 1 site now exists
• extant single plant is probably gt1100 years old!

7
General Principles

• Hybrid frequency (cont.)
• Triploid hybrid woodfern, Dryopteris x
  triploidea, is a common cross of two widely
  distributed North American ferns, D. intermedia
  (4x) and D. carthusiana (2x)
• Hybrid is often more abundant in a given lowland
  forest site than either parent but must be
  constantly recreated de novono ability to
  reproduce!
• Triploid genome confers denser glandular
  hairiness than either parentdosage effect of
  duplicated genome from D. intermedia

8
General Principles

• Hybrids not always restricted to immediate
  vicinity of parents, where vegetative or other
  propagation and dispersal allow
• e.g., Hybrid horsetail, E. x ferrissii, disperses
  by stem fragmentation along waterways far outside
  range of E. laevigatum parent

Raven et al. (1992)
9
General Principles

• Where isolation mechanisms are weak and
  "intermediate" microhabitat for hybrid
  establishment is extensive, hybrid swarms may
  be produced with all forms of phenotypic (and
  potentially physiologically adaptive)
  combinations
• Not rare in plants
• Raw material, with new genotypes, upon which
  selection and other forces may act

10
Hybridization sensu stricto

• Interbreeding halts at sterile F1 or hybrid
  breakdown or other post-mating isolation
  mechanism ? prevents complete interspecific gene
  flow
• Very common in land plantsoperates (or has
  operated) in vast majority of plant groups
• Chromosome doubling or asexual reproduction could
  still produce evolutionarily important products

11
Classic Introgression

• Active and iterative process, occurs after
  initial hybridization event
• Depends on weak interspecific (especially, weak
  post-mating) isolation
• Multigenerational process
• Initial interspecific F1 hybrid produced
• F1 crosses with parent to produce
  first-generation backcross progeny
• Backcross progeny of successive generations
  continue to hybridize with individuals of same
  parent

12
Classic Introgression

• May be bidirectional or unidirectional
• Extent of introgression (and development of
  hybrid swarms) depends on extrinsic factors,
  e.g., site and environmental conditions, as well
  as intrinsic factors, e.g., blooming time of
  parents, nature and strength of isolation
  limiting gene flow between backcrosses and
  parents
• Theoretical consequence is individuals with
  mostly the genome and (exo)phenotype of one
  parent but with some genes of the other parent

13
Classic Introgression

• Most profound impact considered to be
  introgressant plants indistinguishable from one
  parent but with adaptability to broader range of
  environments than either
• Frequency still not fully understood but
  suspected in many groups where hybridization is
  common

14
Classic Introgression

• Evidence for introgression frequently
  demonstrated by comparing nuclear and plastid
  genomes e.g., incongruence between nuclear and
  chloroplast phylogenies of individuals
• Incongruence in genomic phylogenies termed
  plastid capture and is strong evidence of
  hybridization with subsequent introgression
• Sometimes suggests an ancient, cryptic
  introgressive event
• e.g., black cottonwood has nuclear genome of BC
  group but chloroplast of white cottonwood group,
  but has no clear phenotypic traits of the white
  cottonwoods!

15
Classic Introgression
Chloroplast phylogeny
Nuclear phylogeny
P. nigra
P. nigra
Red box white poplar group
Smith Sytsma (1990)
16
Second Introgression Process?

• PhD student Aurea Cortes studied extensively
  hybridizing violet species pairs in Mexico over 3
  field seasons
• Found phenotypic and nuclear genetic marker
  evidence of extensive gene flow ? apparent
  introgression (many parental individuals had
  genetic markers of other parent)
• Found virtually no pollinator movement over 3
  seasons, suggesting that interspecific
  hybridization is rare

17
Pseudo-introgression?

• Violet species have mixed breeding
  system--produce outcrossing showy flowers in
  spring and numerous cleistogamous (strictly
  selfing) flowers later
• Species reproduce largely by cleistogamous
  flowers, hybrid individuals reproduce entirely by
  cleistogamy
• ? meiotic segregation in progeny of hybrids?
• ? is not introgression, which is an active
  backcrossing process
• Needs confirmation, and further study in other
  groups with mixed breeding systems could be
  common?

18
Consequences of Introgression

• True gene flow accomplished across species
  boundaries
• Locally significant if restricted to a particular
  population, but much more significant if it
  occurs to extent that introgressants proliferate
  and disperse widely
• May ultimately affect the competitive ability,
  long-term survival of one or both parental
  species
• May also be complicated by polyploidy, etc.

19
Consequences of Introgression

• May yield a new taxon isolated from either parent
  that is uniquely adapted to a particular set of
  conditions
• Some modern authors use the term "introgression"
  interchangeably to include both hybridization in
  the narrow sense, and introgressionthis is
  sloppy, and the two processes have very different
  evolutionary consequences

20
More on Hybrid Speciation

• Homoploid ("diploid") hybrid speciation
• Parents differ by two or more translocations
  begins with chromosomally sterile hybrid
• Self-fertilization and meiotic recombination
  generates structural homozygote
• Recombinant progeny are true-breeding but yield
  sterile hybrids in progeny-parent crosses
• Could also be accomplished by recombination of
  genic sterility factors (theoretical possibility)
• Experimentally documented in Wild rye
  (Elymus),Gilia (Gilia),Tobacco (Nicotiana), Rice
  (Oryza), etc.

21
More on Hybrid Speciation

• Recombinational speciation through external
  barriers
• ecological speciation following initial
  hybridization
• Parents isolated temporally or ecologically
• Begins with fertile/subfertile hybrid
• Self-fertilization and recombination generates
  externally isolated progeny
• Eventually produces species isolated from parents
• Inferred in amaranth (Amaranthus), larkspur
  (Delphinium), willow-herb (Epilobium), oaks
  (Quercus), etc. proven with molecular data in
  Beardtongues (Penstemon), Wild irises (Iris),
  several other groups

22
More on Hybrid Speciation

• Allopolyploid speciation
• Believed very common in plants--47 of
  angiosperms, 97 of ferns and fern allies
  probably polyploid majority presumably of
  allopolyploid origin
• Begins with a hybrid of two different species or
  "races" (subspecies or varieties)
• Sterile hybrid undergoes chromosome doubling
  (both means below appear to be common events)
• Somatic cells of the stem may generate a
  tetraploid branch that produces tetraploid
  flowers diploid gametes produce tetraploid
  progeny
• Diploid plant produces two sets of unreduced
  (diploid, not haploid) gametes union produces
  tetraploid progeny

23
More on Hybrid Speciation

• Tetraploid is fertile--2 sets of chromosomes
  representing the 2 parental genomes pair up,
  yielding "balanced" gametes
• Famous examples of whole species groups include
  spleenwort ferns (Asplenium), henbit (Galeopsis),
  cotton (Gossypium), wheat (Triticum)
• Multiple origins of allopolyploid species
  documented in many groups, e.g., Goat's-beards
• Maybe more common than we ever thought

24
More on Hybrid Speciation

• Segmental allopolyploidy (older term for
  infraspecific allopolyploidy)
• Series of races of one species hybridize with
  another species in different places
• Chromosome doubling yields a "continuum" of very
  closely related allopolyploids
• Slightly different taxa with same ploidy level
  all interfertile

25
More on Hybrid Speciation

• Factors fostering allopolyploidy
• Long life cycle, with some mode of vegetative
  reproduction
• "Primary" speciation completed, resulting in
  chromosomal rearrangements
• Frequent natural hybridization

26
Bibliography

• Anonymous. Flora of North America Editorial
  Committee (ed.). 1993. Flora of North America
  north of Mexico, vol. 2-Pteridophytes and
  gymnosperms. Oxford University Press, New York,
  New York. 475 pp.
• Briggs, D. and S. M. Walters. 1997. Plant
  variation and evolution, 3rd ed. Cambridge
  University Press, Cambridge, United Kingdom. 512
  pp.
• Futuyma, D. J. 1979. Evolutionary biology.
  Sinauer Associates, Inc., Sunderland,
  Massachusetts. 565 pp.
• Grant, V. 1971. Plant speciation. Columbia
  University Press, New York, New York. 435 pp.

27
Bibliography

• Grant, V. 1991. The evolutionary process A
  critical study of evolutionary theory, 2nd ed.
  Columbia University Press, New York, New York.
  487 pp.
• Raven, P. H., R. F. Evert, and S. E. Eichhorn.
  1992. Biology of plants, 5th ed. Worth
  Publishers, New York, New York. 791 pp.
• Smith, R. L. and K. J. Sytsma. 1990. Evolution of
  Populus nigra (sect. Aigeiros) Introgressive
  hybridization and the chloroplast contribution of
  Populus alba (sect. Populus). American Journal of
  Botany 771176-1187.