Phylogeny, evolution,

development
Georgy Koentges
g.koentges@warwick.ac.uk
 Human skeleton for comparison with that of
birds. Pierre Belon, Nature des oyseaux (The
God had only few ideas.....
nature of birds), Paris 1555
Traditional classification – Linne, Cuvier
• Observation of nested character
states
• No subdivision betweeen ‘old’ and
‘derived’ New characters within
taxonomy
• Binomial classification – the
species is the only stable
taxonomic unit...

Classis 1. MAMMALIA
Classis 2. AVES
Classis 3. AMPHIBIA
Classis 4. PISCES
Classis 5. INSECTA
Classis 6. VERMES
See
http://www.brooklyn.cuny.edu/bc/ahp/CLAS/C
LAS.Linn.html
For a nice intro
From the first growth of the tree, many a limb and branch has
decayed and dropped off; and these fallen branches of
various sizes may represent those whole orders, families, and
genera which have now no living representatives, and which
are known to us only in a fossil state. As we here and there
see a thin, straggling branch springing from a fork low down in
a tree, and which by some chance has been favored and is
still alive on its summit, so we occasionally see an animal like
the Ornithorhynchus (Platypus) or Lepidosiren (
South American lungfish), which in some small degree
connects by its affinities two large branches of life, and which
has apparently been saved from fatal competition by having
inhabited a protected station. As buds give rise by growth to
fresh buds, and these, if vigorous, branch out and overtop on Darwin, 1837
all sides many a feebler branch, so by generation I believe it
has been with the great Tree of Life, which fills with its dead
and broken branches the crust of the earth, and covers the
surface with its ever-branching and beautiful ramifications.
 Two essential parts of
Darwin’s theory

1. Common descent – understanding

Nested similarities between species as left-overs of common ancestors

2. Mechanisms of mutation and selection

Evolution is a long chain of
ontogenies linked together by
the germ-line

Likelihood of transmission of ontogenetic

Information across generations depends on
a. Adaptive traits
b. Sexual selection - # of offspring
c. chance
Von Baer’s ‘law’ - larval stages/embryos are (very often) more
similar to each other than adult stages.

Haeckel’s ‘Recapitulation’

We all have common ancestors

that had similar programmes
already inside

Conservation of developmental
programmes leading to

HOMOLOGY OF
STRUCTURES

common ancestor had processes in place that led to similar features

in descendants
Evolution is chain of ontogenies
PHYLOGENETIC TREES
AND HOW TO CONSTRUCT THEM
Thinking in trees vs bushes...
 What is a character?
Any assayable feature carried at high frq in
population
Not all characters are equally useful to
reconstruct trees –
Hennig (Phylogenetic Systematics) figured out
that only synapomorphic ones are informative
for tree structure. <-> phenetics accepts all...
http://books.google.co.uk/books?
Here is his famous 1966 book hl=en&lr=&id=xsi6QcQPJGkC&oi=fnd&pg=PA1
Phylogenetic Systematics: &dq=hennig+phylogenetic+systematics&ots=Q
sKCkvGC5S&sig=fvLeM85iVW5_i1GnoRrGvRxo
x1A#v=onepage&q&f=false
 Relative terms in triad:
Sister groups

outgroup

C D

Paraphyletic B
Grouping
(does not include A (syn)apomorphy = new
all character only shared
Descendants of a between C and D sister
common groups and no other
Ancestor) grouping

Plesiomorphy = older
Character shared by several
taxa
 Definitions
• Monophyletic group = group of all taxa derived
from a common ancestor, including this ancestor
• Stem group – ancestral taxon of monophyletic
group not shared with other monoph grouping

• Sister groups – two taxa more related to each

other than either to a third taxon
• This is the Outgroup in this case
 Characters for tree reconstruction
(syn)apomorphy Only synapomorphies can be used (Hennig)
plesiomorphy
Sister groups

B C D B C D B D
C
 Characters for tree reconstruction
(syn)apomorphy
Only synapomorphies can be used (Hennig)
plesiomorphy But these might be hard to determine – now cladistics helps!

Sister groups

B C D B C D B C D

gain
gain
gain loss loss

gain gain

autapomorphy

Parsimony: Minimize number of transitions within tree – Occam’s razor

 Emergence of cladistics
Numerical methods to establish
relationships

From http://fossilnews.com/1996/cladistics.html
 Many computational approaches
are now used to calculate most parsimonious
trees, based on data matrices obtained from
morphology or DNA sequences

Neighbor-joining is an iterative algorithm. Each

iteration consists of the following steps:
1. Based on the current distance matrix calculate
the matrix Q (defined below).
2.Find the pair of taxa in Q with the lowest value.
3.Create a node on the tree that joins these two
taxa (i.e., join the closest neighbors, as the
algorithm name implies).
4.Calculate the distance of each of the taxa in the
pair to this new node.
5.Calculate the distance of all taxa outside of this
pair to the new node.
6.Start the algorithm again, considering the pair of
joined neighbors as a single taxon and using the
distances calculated in the previous step.
now let’s add in the fossils
Now consider, how new fossil evidence can change the way
We interpret the sequence of evolutionary events.
1. We start with establishing a tree with monophyletic groups.
2. We map characters into a tree and infer from outgroups primitive conditions.
3. We extend our knowledge about ancient character states by mapping older taxa

A B C

Secondary loss
gain
F
E
character not present primitively
D

Character *was* present primitively

Therefore, more information about ancient character states can change the polarity
of character changes (i.e. when they were lost or new characters form in the tree)
 total gnathostomes

living

LCA (last common

ancestor)

) stem groups
outgroup

jawed placoderms

Crown+Stem = Total group

jawless osteostracans

Crown groups comprise the last common ancestor of a group of living species plus all of its descendants, both
fossil and modern. = same definition as monophyletic group
The gnathostome crown group includes the last common ancestor of osteichthyans (represented by a salmon) and chondrichthyans (represented by a
shark) plus all of its descendants, and comprises all the green and orange parts of the tree.
Total groups include the crown group of interest plus all extinct forms more closely related to
that lineage than any other living species. Here, the gnathostome total group is represented by all
coloured parts of the tree. Stem groups are equal to a clade’s total group minus its crown group,
shown here by the pink lineage connecting the vertebrate and gnathostome crown nodes. Jawed vertebrates include all of the gnathostome crown,
and the upper reaches of the gnathostome stem. The lower part of the gnathostome stem is populated by jawless ostracoderms, which are more
closely related to jawed vertebrates than they are to modern jawless fishes. The principal task faced by palaeontologists is to fit fossil groups (like
acanthodians and placoderms; ‘†’ indicates they are extinct) within the genealogical framework for modern species 
 Character evolution
• First establish a parsimonious set of equally
likely trees on a large set of features
• Then you can map characters and their
changes onto the tree
• Then you can start determining the molecular
mechanisms underlying these changes.

- In this order.
Characters for tree reconstruction
Only synapomorphies can be used (hennig)

(syn)apomorphy
plesiomorphy
Sister groups

B C D

Fossils
Give us this
Information!!!
Stem group
Features in stem group but lost in
C,D lineages
 The extant phylogenetic bracket as inferential tool when dealing
with ancient or inaccessible organisms –you can reconstruct
soft tissues, genomic sequences etc of shared common ancestor!

Koentges
How can we trace the
sources of similarity/homology?

Study character evolution

use plesiomorphic genetic
features to label common
(homologous) populations
of cells

Koentges
Constraints on mutational change:
forces of conservation
• Developmental/genetic coupling of different
features as their development uses the same
genes and pathways. Genes as ‘tools’ –
pleiotropy of gene action
• common cell populations
• Important genes/pathways don’t get
modulated much through mutations
What new information can fossils
bring?
They provide a structural richness that remains to be explained
mechanistically
The Evo-Devo field is born.
What fossils can tell us that extant comparisons
cannot..surprising Character states and transitions
in extinct stem groups...

Acanthostega

early
crown tet
stem tets

amniotes

It gives us something to explain!

Deciphering gene regulatory
History:
• What stays the same
• What changes – how? Largely regulatory
changes
• Functional and intragenomic constraints due
to pleiotropy of gene action
• Chance/stochastic effects fixate particular new
character states within populations
Hox genes as master ‘address code system’
Hox genes newly used in amniotes as address codes of vertebra ‘identity’
Vertebrae types directly correlate with the prior gene expression domains of Hox genes
Across different vertebrate species – thus, changes in expression domains could
generate diverse morphologies...
Hox genes in lateral plate
mesoderm
 Somites: musculature (muscle cells) of limbs

Lateral plate mesoderm: skeleton, tendons of limbs

All of this is a mesenchyme in the early embryonic limb bud which gets
Regionalized first along anterio-posterior and dorsoventral axes.

From Zeller paper – READ THIS ESSENTIAL REVIEW!

 Stylopod humerus upper arm/thigh
Zeugopod= radius/ulna (lower arm) or tibia/fibula (calf)
Autopod = hand and foot AER: apical
Ectodermal ridge

Progress zone: proliferating zone, dependent upon AER for growth and specification
Temporal code becomes a spatial code
From Zeller paper – READ THIS ESSENTIAL REVIEW!
 Dorsal unpaired fins
lampreys

Origins of fins –

Unpaired vs paired

First paired fins emerge

Fin appendages with digits in tetrapods

Hox genes are first expressed in the CNS, somites and unpaired fins
Paired fins evolved after unpaired fins
Later in evolution Hox gene codes are coopted to the paired fins and are used to
subdivide them molecularly:
=> Cooption of a molecular programme from one body region to another!

lampreys shark
Osteichthyans
(all other vertebrates)

NATURE|Vol 442|31 August 2006

Cooption of same
programme in
Paired fins

Dorsal fin hox

Gene programme

NATURE|Vol 442|31 August 2006

Digit evolution and development
What fossils can tell us that extant comparisons
cannot..surprising Character states and transitions
in extinct stem groups...

Acanthostega

early
crown tet
stem tets

amniotes

It gives us something to explain!

Anchoring of the pelvic fin onto the vertebral column – evolution of the
Pelvic girdle

http://beta.revealedsingularity.net/article.php?art=tetrapod_evo
Colinearity of hox gene=

Position + time &

Space of gene expression

Cooption of
nested Hox gene
expression into
paired
appendages
 Cluster position determines
proximo-distal position and
timing of Hox gene expression

Late expression domains are

Used for the formation of
Digits....another tetrapod novelty
Colinearity of Hox gene
Position and expression domain
Explaining evolutionary
patterns of digit changes
mechanistically
temporal axis turns into physical axis: digits form and individualize last!
Late blockage will prevent individuation of fingers – yielding paddles/flippers!
 Digits

The expression domain of the HoxD13

paralogs
Sets up the territory for digits of the
autopod!
Shifts in that domain in evolution change
number and shape of digits.

THESE SHIFTS ARE PART OF THE

SECOND WAVE OF HOX
EXPRESSION
 A NEW MODEL FOR THE EARLIEST TETRAPOD LIMBS

Changing of Hox +Gli

gene dosage:
Change in digit
numbers

Acanthostega Evolutionary limb activation of GLI3+ HOXD11-13

Led to restriction of fingers to 5! –
and finger polarity (thumb vs pinky)
 Tetrapod
Permanently
terrestrial

6-7 digits

5 digits

Shh! Stepwise expression

change
Of Hox genes +
responsiveness to
shh signalling
 Modification of the pentadactyl
limb in amniotes
Progress zone

CHANGING
LATE STAGES OF
PROGRESS ZONE
ONLY AFFECTS
THE DIGITS
 Secondary loss of finger identity
secondary loss of the pelvis connection…
 http://fossil.wikia.com/wiki/Ichthyosaur

http://www.ucmp.berkeley.edu/people/
motani/ichthyo/forefin.html

Explained as stepwise losses (or gains) of embryonic signalling processes (shh)

Figure 2. Click to enlarge. The origin of the pterosaur wing and the migration of the pteroid and preaxial carpal. A. Sphenodon.
Huehuecuetzpalli. C. Cosesaurus. D. Sharovipteryx. E. Longisquama. F-H. The Milan specimen MPUM 6009, a basal pterosaur.
Re-use of Hox genes in therian mammals to
differentiate/subdivide
Reproductive organs
Uterus and Vagina are novelties of placentals. These differentiated at the base of the
Mammals.

Uterus
cloaca
vagina
These placental novelties: Uterus, Vagina (and their respective sizes) are organized by
posterior Hox genes (HoxD10-13).
The same genes also regulate penis and finger
size at the same time...

Thus, Hox genes explain at least one key aspect

Of our current international politics...

Lynch VJ, Roth JJ, Takahashi K, Dunn CW, Nonaka DF, Stopper GF, Wagner GP (2004) Adaptive evolution of HoxA-11 and HoxA-13 at the origin of the uterus in
mammals. Proc Biol Sci. 271(1554):2201-7.
Wagner GP, Lynch VJ (2005) Molecular evolution of evolutionary novelties: the vagina and uterus of therian mammals. J Exp Zoolog B Mol Dev Evol.
• Pleiotropy of gene action – digits and penises
• Developmental coupling of different features
through the shared action of the same gene(s)
Phylogeny as a chain of related
ontogenies – with evolutionary
modification

How?
 Mechanistic concept underpinning
character evolution
CRMs (cis-regulatory modules, enhancers, silencers)
Modular control units of gene expression

Evolutionary changes

Spatial expression
(cell type? where?)

Temporal expression
(when in development?)
Gene or gene cluster

Structural evolution that we discover when
Placing characters into phylogenetic trees
Hox genes:
Co-option from AP axis from dorsal fin -
mesoderm
Cooption from fin mesoderm to to paired fin
mesoderm
Refinement, responsiveness to shh signalling
Co-option to reproductive organs