Learning objectives

By the end you should be able to:

• List the major modes of plant speciation and their genomic signatures.
• Explain why polyploidy and hybridization receive special attention in plants.
• Connect biological mechanisms to earlier popgen concepts.

An extension of population genetics

1. Individuals can be grouped into population
2. Populations can be grouped into species
3. Species evolve to give rise to new species
4. New species arise through four speciation models:

• Two emphasize geographic isolation (allopatric and peripatric)
• Two emphasize the breakdown of gene flow without geographic isolation (sympatric and parapatric)

Biological Species Concept

• Biological Species Concept (BSC): species are groups of interbreeding natural populations that are reproductively isolated from other such groups. There are two components:
  1. Gene flow is maintained among populations within the species
  2. Gene flow is negligible between populations of different species

Component 2 is often more meaningful for plants. Some species may hybridize freely and but are geographically disjunct and have little opportunity for gene flow.

Vicariant Speciation

• Vicariance: a form of allopatric speciation where a physical barrier splits a population, leading to reproductive isolation over time.
• Allopatric Speciation: new species arise when populations are geographically separated.
• Peripatric Speciation: a form of allopatric speciation where a small population becomes isolated at the edge of a larger population’s range, leading to rapid divergence.

Both cases involve: - Subpopulations becoming genetically distinct - Selection leading to genotypic or phenotypic differences that preclude interbreeding.

Vicariant Speciation

Geographic isolation creates barriers to gene flow. Well demonstrated by the Hawaiian islands.

• largest number of endemic plant species in any one geographic region.
• endemic species: evolved in a location and found nowhere else
• native species: arrived from somewhere else but established among the flora

Vicariant Speciation

Data from Wagner, Herbst, and Sohmer (1990)

Vicariant Speciation

Hawaiian islands are volcanic islands. New islands emerge with no species, followed by colonization from older islands and subsequent speciation events.

Age of Hawaiian islands. Fig. 1 from Landis, Freyman, and Baldwin (2018)

Vicariant Speciation

The silverswoard alliance (Argyroxiphium, Dubautia, Wilkesia) in the Hawaiian islands is a classic example of adaptive radiation, where likely a single colonizing species gives rise to multiple species adapted to different ecological niches.

Argyroxiphium sandwicense (A) and related species. Fig. 3 from Baldwin and Wagner (2010)

Vicariant Speciation

The most likely biogeographic model supports a single origin on the oldest Hawaiian island, Kauai, followed by dispersal to younger islands and subsequent speciation events.

Support for different models of colonization from North America and silverword alliance diversification. Fig. 4 from Landis, Freyman, and Baldwin (2018)

Islands Everywhere

Andean uplift occured over time creating many opportunities for specication

Andean uplift and speciation opportunities. Fig. 1 from Hazzi et al. (2018)

Islands Everywhere

Andean uplift occured over time creating many opportunities for specication

Andean uplift and speciation opportunities. Fig. 3 from Hazzi et al. (2018)

Islands Everywhere

Andean uplift occured over time creating many opportunities for specication

Andean uplift and speciation opportunities. Fig. 2 from Pérez-Escobar et al. (2022)

Other barriers to gene flow

• Prezygotic: Barriers to mating or fertilization of eggs
  1. Geographical
  2. Temporal: example is flowering time
  3. Mechanical: example is pollen pistil interaction
  4. Gametic Incompatibility: example is that sperm and egg do not fuse from a gex2 mutant
• Postzygotic: Barriers to the formation of viable hybrids
  1. Hybrid inviability: example is endosperm failure terminates the hybrid
  2. Hybrid sterility: Reproductive organs do not develop
  3. Hybrid breakdown: The F1 is doing great but the F2s have reduced fitness

Example: pollen-pistil interactions

Pollen-pistil interactions. Fig. 1 from Wheeler, Franklin-Tong, and Franklin (2001)

Example: pollen-pistil interactions

A case study from Taraxacum (dandelion) species.

Pollen-pistil interactions in Taraxacum. Fig. 2 from Nishida et al. (2014)

Example: endosperm failure

Sperm and egg fuse to make the 2n gamete, but the 3n endosperm is needed for proper seed development. Endosperm development usually needs a 2:1 maternal to paternal genome ratio.

Scematic of double fertilization in plants. Fig. 1 from Dresselhaus, Sprunck, and Wessel (2016)

Example: endosperm failure

Sometimes, hybrid seeds lead to dosage imbalances.

Data from LESTER and KANG (1998)

Example: endosperm failure

Image of failed endosperm from Fig. 1 of LESTER and KANG (1998)

Example: hybrid sterility

In 1927, Georgi D. Karpenchenko (1899-1941) attempted to to hybridize the common radish (Raphanus sativus) with the cabbage (Brassica oleracea). Both parents have a base chromosome number of 9, so the diploid is 2n=18. The hybrids had 2n=9!

Parental chromosomes were too diverged to pair properly during meiosis. The mispairing resulted in hybrid sterility.

Overcoming barriers

However, a very small proportion of hybrid offspring were not sterile. These has 2n=36 chromosomes! Formed where there was a spontaneous chromsome number doubling in the germline. Backcrossing was not possible.

Highly variable phenotypic outcomes and not a useful crop, but a demonstration of how polyploidy can overcome hybrid sterility.

Examples of Raphanobrassica, resynthesized by McNaughton (1973)

Non-vicariant speciation

• No requirement of isolation by geographic barriers
• Sympatric speciation — speciation occurring within the same geographic area, often driven by ecological or behavioral factors.
• Parapatric speciation — speciation occurring in adjacent geographic areas, with some gene flow between populations.

Karpechenko’s work and the past 100 years of science have shown plants have the potential to form new species rapidly without geographic isolation.

Sympatric speciation through polyploidization

Autopolyploidy through either: 1. Meiotic nondisjunction 2. Mitotic nondisjunction in the zygote

Example: Autopolyploidy in Galax urceolata

Autopolyploidy is considered to be uncommon. Stebbins considered Galax urceolata to be one of the better examples. Tetraploids are distributed primarily across the Blue Ridge.

The Galax urceolata distribution, showing tetraploid individuals across the Blue Ridge, from Servick et al. (2015)

Sympatric speciation through polyploidization

Allopolyploidy involves hybridization between two species and can happen through: 1. Spontaneous doubling of an otherwise inviable hybrid 2. A triploid bridge that backcrosses with a parent

Example: Allopolyploidy in Tragopogon

Allopolyploidy in Tragopogon, from Soltis and Soltis (2009)

The triploid bridge

Cartoon of how polyploids can form, from Rieseberg and Willis (2007)

Ploidy from a species perspective

Differentiating types of hybridization and polyploidy, from Soltis and Soltis (2009)

Are allopolyploids more common than autopolyploids?

The data suggests no, but more allopolyploids are accepted species

The relative frequency of auto versus allopolyploidy across plants. Fig. 1 from Barker et al. (2016)

Getting around the endosperm failure problem

No pollen no problem. Asexual reproduction can bypass the endosperm failure that often occurs in interspecific crosses.

Getting around the endosperm failure problem. Fig. 1 from Hörandl (2024)

Apmicts are frequenctly polyploids, but not always.

Example: Apomixis in polyploid Ranunculus

Polyploids likely formed in diploid range but found success by filling a new niche.

Getting around the endosperm failure problem. Fig. 1 from Karbstein et al. (2022)

Apmicts are frequenctly polyploids, but not always.

Parapatric speciation

• Need not invoke chromosomal mechansisms, but consider speciation with geneflow between partially connected populations.
• A hybrid zone can backgross genes into parental populations
• The pieces of the genome that remain over time may serve adaptive purposes

Parapatric speciation

Reinforcement: when hybrids are less fit and prezygotic barriers might encourage conspecific mating.

Cartoon of reinforcement in parapatric speciation. Fig. 1 from Long et al. (2026)

Estimating ploidy

Ploidy can be estimated using several methods, including: - Flow cytometry: measures the DNA content of nuclei. - Chromosome counting: direct observation of chromosomes under a microscope. - Molecular markers: can infer ploidy based on allele dosage. - Morphological traits: sometimes correlated with ploidy, though less reliable.

Estimating ploidy with flow cytometry

Estimating ploidy with flow cytometry. Unpublished data

Estimating ploidy with flow cytometry

Estimating ploidy with flow cytometry. Unpublished data

Perspectives on how long until speciation

Waiting for neutral processes and isoaltion to work can take a long time. Polyploidy and hybridization might be adventageous under changing environmental conditions.

Perspective on the time required for speciation through different mechanisms. Fig. 1 from Levin (2019)

Summary

• For types of plants speciation models
• Non-vicariant processes important for plants
• Life history evolution is feasible