Network (Reticulate) Evolution:
Biology, Models, and Algorithms
C. Randal Linder*, Bernard M.E. Moret†
*University
of Texas at Austin
(currently the Program for Evolutionary Dynamics,
Harvard University)
†University
of New Mexico
Purpose of Tutorial
• Familiarize you with the nature of reticulation
in biology, especially hybrid speciation
• Discuss the implications of reticulation for our
understanding of evolution
• Present currently available methods for
simulating, detecting and reconstructing
reticulation
• Consider deficiencies of the current methods
Overview of Reticulation in Biology
• What happens at the genetic level?
• How does it relate to population genetic
processes?
– In particular, what processes can give the
appearance of species level reticulation
• How can we detect it?
• How can we reconstruct it?
• What biological tools need to be in place to
generate the requisite data?
Idealized Nature
• Wouldn’t it be nice if…
– Sexual creatures would just behave
themselves
– Asexual lineages would keep their
pseudopods to themselves
Then we could stick with bifurcating
graphs (trees) to properly describe
the evolutionary history of
organismal lineages
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Unruly Nature
Whatever is not forbidden will
occur.
-- Gerald Myers
(ca 1980)
In Other Words
• Nature does not care about our nice systems
• Rather, the only rule is:
– If a set of genes can be brought together in a cell,
survival and reproduction will be determined by the
phenotype produced in the environment of the
organism.
• If the organism can survive and reproduce as
well as or better than its competitors, it
“works” no matter the mating/process that
produced it
Therefore
• Some “species” are able to interbreed or
exchange genes in ways that violate
“normal” notions about species and
speciation
• Reticulation is violation of the
independence of each evolutionary
lineage
– Instead of bifurcation, lineages can mix and
produce new lineages
• This leads to the production of networks
instead of trees
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I
Molecular phylogeneticists will have failed
to find the “true tree,” not because their
methods are inadequate or because they
have chosen the wrong genes, but
because the history of life cannot
properly be represented as a tree.
--Ford Doolittle
Before Reticulation
• Paradoxically, I’ll begin with non-reticulate evolution
• Bifurcating evolution (and sometimes hard
polytomies)
– Evolutionary lineages split and evolve independently from
one another
Before Reticulation
• Key Evolutionary Insight: Because all evolution is a
product of change from one generation to the next,
the information must initially change in some form of
bifurcating process.
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With Reticulation
• The end result is admixture of
different evolutionary histories
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Levels of Reticulation
• Life is organized hierarchically and so
reticulation can occur at different levels
– Chromosomal (meiotic recombination)
– Population (sexual recombination)
– Species (interspecific hybridization and
horizontal gene transfer)
Levels of Reticulation
• Chromosomal (meiotic recombination)
Levels of Reticulation
Population (sexual recombination of haploid genomes)
Levels of Reticulation
• Species (hybridization and gene transfer)
Levels Nested within Levels
Areas of Biological Research
• Most of the work on reticulation has been
done at the population genetic level
– A great deal of work on recombination,
especially meiotic recombination
• Hybrid speciation and lateral gene
transfer are less well studied
– Intersect with the population genetic
perspective
– Will talk about this a bit later and from other
speakers
Types of Hybrid Speciation
• Allopolyploidization: each parent of the hybrid contributes
it’s entire nuclear genome (usually uniparental inheritance
of the organelles)
– Parents needn’t have the same number of chromosomes
Types of Hybrid Speciation
• Diploid (Homoploid) Hybridization: each parent
contributes half of its diploid chromosome set, as it
would with normal sex.
– Parents almost always have the same number of
chromosomes
Types of Hybrid Speciation
• Autopolyploidization: a doubling of the diploid
chromosome number in a single species
– From a biological and topological perspective, could be
considered a type of bifurcating speciation
Horizontal Gene Transfer
• Hybridization between lineages, but
an independent lineage is not
produced
– Hybrids backcross to one or both
parents allowing introgression of genes
between “species”
• Genes are moved between lineages
by a third party (vector), e.g., a virus
Horizontal Gene Transfer:
Introgressive Hybridization
Horizontal Gene Transfer:
Genome Capture
• A complete organellar genome is
transferred by hybridization
Horizontal Gene Transfer:
Bacterial Sex
• Genetic material
is moved by
conjugation
between
compatible
bacteria
Bacteria: Promiscuous DNA Sharers
• Lawrence, Ochman estimated that 755 of 4,288
ORFs in E. coli were from at least 234 lateral
gene transfer events (Proc. Natl Acad. Sci. USA 95,
9413-9417 (1998) )
• General evidence:
Horizontal Gene Transfer:
Exchange by a Vector
• Genetic material
is moved by a
third party such
as a virus or a
combination of
organisms, e.g.,
mosquito and
protozoan.
Neworks Have Incongruent
Trees Within Them
Reticulation Events Have
Incongruent Trees Within Them
Reticulation Events Have
Incongruent Trees Within Them
Fundamental Insight
• At the lowest possible level
(individual DNA nucleotides on a
single DNA strand) all evolution is
ultimately tree-like.
How Might We Detect
Reticulation?
• Fundamentally, reticulation is a mixing of
different evolutionary signals. Therefore:
– The signal from a genome that has
experienced reticulation will be an “average”
of its parents (Median approach)
– Unrecombined stretches of DNA will have a
signal that comes from one parent.
(Incongruence approach)
• Will see both approaches in methods for
detection and reconstruction
Evolutionary Events that Mimic
Species-Level Reticulation
• Lineage Sorting (gene tree/species tree
problem)
• Reticulation at lower levels, e.g., meiotic
recombination
Evolutionary Events that Mimic
Species-Level Reticulation
• Lineage Sorting (gene tree/species tree
problem)
– When reconstructing a species-level
phylogeny using DNA sequence information
we are actually reconstructing a gene tree.
– Ancient alleles (alleles arising prior to some
monophyletic group) may not be inherited
by all species.
– In essence, it is either a sampling problem
or an irretrievable information loss problem.
Gene Tree/Species Tree
Gene Tree/Species Tree
• All of the versions of a gene from a single common history
(everything that is the same color) are referred to as
orthologues.
• Versions of a gene from a duplication event or the
production of a new allele are paralogues
Gene Tree/Species Tree
Gene Tree/Species Tree
Gene Tree/Species Tree
Gene Tree/Species Tree
Gene Tree/Species Tree
Gene Tree/Species Tree
Gene Tree/Species Tree
• Under a molecular clock, it is possible to detect the
difference between incongruence due to hybridization and
to a gene tree/species tree sampling problem.
•GT/ST incongruences will occur at different depths.
Evolutionary Events that Mimic
Species-Level Reticulation
• Reticulation at lower levels, e.g., meiotic
recombination
– Recombination can lead to loss of an allele
for a lineage in a particular region of DNA
essentially giving rise to a lineage sorting
problem.
Recombination Example
Second Key Insight
• Events that masquerade as species-level
reticulate evolution are always the
product of either true data loss or
inadequate sampling.
– Here, we encounter the importance of a
population genetic perspective in
phylogenetics.
Given the problem of
misleading signals, how can
we distinguish true specieslevel reticulation from
reticulation at other levels,
simple data loss, and
inadequate sampling?
Possible Solution
• Increase the number of individuals
sampled from a species/population and
the number of markers.
• Therefore, must take a multiple marker
approach to recovering the specieslevel relationships
– Data loss and lower level reticulation
events should almost always act randomly
with respect to which phylogeny is favored
– Species-level reticulation will be biased
toward a particular interpretation
Practical Concerns
• Practical problems (for biologists):
– Cost
– Time
– Lack of prior knowledge that all of the
orthologues are there to be found
Caveats
• Reticulation events that quickly follow
speciation may not be detectable
• Ancient reticulation events may not be
recoverable
• The computational requirements to
detect and reconstruct reticulation may
be considerable
• We may have to rethink our ideas of species
(levels/units of speciation)
Assembling the Network of
Life: ANOL