Epigenetic factors in evolution


A few examples on the epigenetic nature of
transgenerational plasticity (antibiotic resistance
in bacteria, doubling of the size of the helmet in
the offspring of D. cucullata, appearance of the
new morphological and physiological traits in the
offspring during phase transition in locusts, and
production of males and females with associating
changes in morphology and physiology, from the
all-female crustacean Daphnia magna) presented
in the first post of this series remained unchallenged,
what may be reasonably considered as a consensus
exists here in TO on the epigenetic origin of the
transgenerational developmental plasticity.

For those who may still not be convinced that
epigenetic factors and epigenetic inheritance plays
a role in evolution, I will provide a few examples
of epigenetic determination of evolutionary changes
in nature and laboratory. I will use conclusions from
leading investigators of the evolutionary changes
on their nature (genetic or epigenetic) to the greatest
possible extent.

Cortical inheritance in Ciliates

From their studies on cortical inheritance,
investigators came to the conclusion that
"For all cortical traits examined, development is
hereditarily determined by existing and
self-reproducing cortical arrangements: the
genes (or DNA) doubtless control synthesis of the
molecular building blocks, but not their site of
assembly or the position, orientation and number
of assemblies" (Sonneborn, T. 1970. Gene Action
in Development. Proceedings of the Royal Society
London B Series Biological Sciences 176: 347-366).
Later experimenters have confirmed the cortical
inheritance but no experiment has disproved it.
Under such circumstances it was concluded that
“A cell possesses (at least) two classes of structural
information: information linearly coded in nucleic
templates, either nuclear or cytoplasmic, and
information encoded in supra-molecular
organization” (Nanney, D.L. 1966. Corticotype
Transmission in Tetrahymena. Genetics 54: 955-968).

The evolution of the body size in Manduca sexta.

In the course of 30 years, or about 220 generations,
this insect evolved a 50% increase in body size
and investigators have found that 90% of the
evolutionary change is result of epigenetic factors
(D’Amico et al., 2001).
Investigators came to the conclusion that no
mutational changes but changes in three epigenetic
factors: growth rate, critical weight and timing of
secretion of neurohormone PTTH “almost
completely account for the evolutionary
increase in body size observed.” (D’Amico et al., 2001;
Davidowitz et al., 2003; Davidowitz et al., 2004).

Evolution of caste polymorphism in ants

Social insects have castes consisting of individuals
of distinct morphology and behavior, with the
latter acting as a biological glue for holding the
colony together as a functional unit.
Experiments with winged and wingless castes of
Pheidole morrisi have shown that the
developmental pathway for wings consists of three
switch points; the first one that determines
development of queens and workers depends on
the level of maternal JH during oogenesis. The
second depends on the external stimuli (photoperiod
and temperature), to which the embryo responds by
generating brain signals (allatotropins/allatostatins)
that regulate production of juvenile hormone (JH).
Pulses of JH determine production of (winged)
queens, whereas lack of JH pulse determines
formation of worker and soldier larvae.
There is only one known mechanism of regulation
of JH in insects and this is a neural mechanism
that starts in the CNS with secretion of
neurohormones, allatotropins, and allatostatin
that stimulate and inhibit synthesis of JH,
respectively.
Empirical evidence has shown that the initial
differentiation of the queen line from the worker
lines is determined by a first JH pulse during the
early embryonic development and the differentiation
of the major workers from minor workers is
determined by a second JH pulse taking place during
larval development in the minor worker line.
The wing disc that develops in presumptive major
workers is later eliminated by apoptosis. Both JH
secretion and the programmed cell death in insects
are neurally determined by signal cascades that start
in the insect brain, as a result of the processing of
external and internal stimuli.

Evolution of limbs in tetrapods

Investigators have found no evidence, and even no
indication whatsoever, of any relevant change in the
structure or function of the key genes for limb
development. On the contrary, ever-increasing
evidence shows that not only key genes for limb
development (Fgfs, Shh, Hoxb8, BMPs, etc.) but
the whole gene regulatory network (GRN) for limb
development is functionally conserved among
vertebrate and invertebrate metazoans (Abouheif,
1999).
Limb development in tetrapods involves also
changes in the neurohormonal regulation and the
ctivity of the respective spinal cord and nerves from
brachial plexus (Wehrle-Haller et al., 1991, McCaffery
and Dräger 1991; Tanaka et al. 1996).
The early stages of development of the fish fins
and the tetrapod limbs show a common pattern of
development and only later changes in the patterns
of expression of key genes for limb development
determine formation of the tetrapod limb.

“Changes in the temporal expression, spatial
expression and level of expression of key
developmental regulators such as BMP and Fgf
appear to be important in driving the evolution of
vertebrate limbs” (Weatherbee et al., 2006)

Loss of eyes in Astyanax mexicanus
The cave-dwelling form of the fish Astyanax
mexicanus lost its eyes probably during the last
12,000 years. W. Jeffery, the leading investigators
of the fish writes:

“Gene expression data suggest that loss of function
mutations have not occurred in cavefish eye genes,
including those structural genes that function at the
bottom of regulatory cascades....lens transplantation
indicates that cavefish have the capacity to form a
complete eye and that they posses and are capable of
using all the genetic factors necessary for later eye
development...The developmental evidence does not
support an evolutionary model that proposes loss of
function of the genes involved in the early development
and/or eradication of the embryonic eye to conserve
energy" (Jeffery, W.R. 2005. Adaptive Evolution of
Eye Degeneration in the Mexican Blind Cavefish.
Journal of Heredity 96: 185-196).
The fact the experimental transplantation of the
lens vesicle of epigean eyed fish to the embryos
of blind cave morph induces the development of
eye structures in the latter, clearly shows that the
eyeless fishes have all the genes necesssary for
eye development during embryogenesis.
Jeffery's conclusion is also confirmed by the fact
that exposure of the larvae of the eyed, eyeless,
and hybrid forms of A. mexicanus to light or
darkness for one month leads to dramatic phenotypic
changes such as development of eyes in the eyeless
form and enlargement of eyes in the eyed form,
suggesting that the photic stimulus influences the
developmental pathways of eye formation (Romero
and Green, 2005).

Loss of dentition in birds
Birds lost dentition some 80 million years ago.
However, they have in place (and functional) all the
odontogenic genes involved in odontogenesis. This
was proven in experiments by Kollar and Fisher
(1980), who by combining the chick presumptive
embryonic epithelium with mouse molar
mesenchyme of neural crest origin observed
development of in chicks structures similar to
mouse teeth and concluded that loss of teeth in
birds is not related to changes in genetic information.
In their interpretation these experiments have
shown that:

“The ability of chick epithelium to participate in
odontogenesis and to secrete enamel matrix protein
suggests that during evolution avian toothlessness
was not a consequence of a change in the genetic
coding in the oral epithelium for specific protein
synthesis that persists in Reptilia and Mammalia.
Rather, an upset of a developmental sequence or an
alteration in the behavior of the cranial neural crest
cells must have blocked the initiation of tooth
development and subsequent synthesis of enamel
matrix proteins....These data provide evidence that
phenotypic change in evolution need not involve
loss of genetic information (Kollar, E.J. and Fisher,
C.1980. Tooth Induction in Chick Epithelium:
Expression of Quiescent Genes for Enamel
Synthesis. Science 207: 93-95).
The fact that in more recent experiments teeth
formation was induced in chicks by homotopic
transplantation of the mouse cranial neural crest
cells in chicks (Mitsiadis, T.A. et al. 2003.
Development of teeth in chick embryos after mouse
neural crest transplantations. Proceedings of the
National academy of Sciences USA 100: 6541-6545)
confirms the results of the earlier experiments that
the loss of teeth in birds is result of the fact that the
bird neural crest cells lost the epigenetic capability
of inducing expression of BMP4 and SHH in
tooth-forming sites of the chick oral epithelium
(while these genes are normally expressed in other
tissues and organs).
The chick chimerae form teeth of the donor of
the neural tube (mouse) suggesting that the mouse
neural crest cells are provided with instructions
(epigenetic information) for inducing ontogenesis
before they leave the mouse neural tube.

“It is tempting to speculate that the different
properties of the mandibular and maxillary
ectomesenchymal cells are related to different
origins of the neural crest cells that populate
these components of the first branchial arch.
Fate mapping in avian and mouse embryos
shows that the mandible is mainly composed of
CNC cells that migrate from the midbrain with
some contribution from rhombomeres 1 and 2.
The maxillary ectomesenchymal cells are derived
from CNC cells migrating from both the midbrain
and the forebrain. Such a difference in axial origin
might explain the different responses of these cells
to epithelial signals.” (Ferguson et al., 2000)

Loss of metamorphosis in salamanders

Metamorphosis in salamanders is stimulated by a
surge in the level of the hormone thyroxine
determined by a signal cascade that starts in the
salamander’s brain (neurons of the hypothalamic
paraventricular nucleus secrete TRH (thyrotropic
releasing hormone)→ neurons of the pituitary secrete
TSH (thyroid stimulating hormone) → Thyroid gland
secretes T4+T3 → Thyroid hormones bind their
nuclear receptors starting metamorphosis processes
(fin elimination, skin changes, etc.).
The timing of the activation of the cascade is
determined by the

“hypothalamic maturation comprising neurons of
several regulatory centers and culminating at the
time of the secretory surge.” (Rosenkilde and
Ussing, 1996).

Paedomorphic salamanders fail to generate the
characteristic burst of hypothalamic stimulation
for activating the thyroid axis. This seems
to be the main mechanism behind the axolotl
paedomorphosis (Rosenkilde and Ussing, 1996).

Metamorphosis has been experimentally induced
in paedomorphic salamanders by administration
of thyroid hormones but it can also be induced
by manipulations at every level of the
neurohormonal cascade. In addition to
neurohormonal manipulations, experimental
metamorphosis in paedomorphic salamanders
is induced by stressful conditions (capture
stress and conditions of captivity), which cause
general disturbance in the central nervous system,
or by increasing the environmental temperature
(Rosenkilde and Ussing, 1996).
Cases of spontaneous metamorphosis in
paedomorphic salamanders have also been reported,
corroborating the idea that no changes in genes
have been necessary for transition from
metamorphosis to paedomorphosis and vice versa.

Why these neurons do not respond to the production
of thyroxine in paedomorphic salamanders?
Hypothalamic neurons self-activate and secrete
TRH in response to low premetamorphic levels of
thyroxine. The fact that they do not respond that
way in the case of paedomorphic salamanders
suggests that the hypothalamus may have
adaptively heightened the set point for responding
to the hormone. The changes in set points are a
well known epigenetic function of hypothalamus
in vertebrates.

All the elements of the neurohormonal cascade are
functional and the loss of metamorphosis is
determined by an epigenetic change in the setpoint
that hypothalamus determines for thyroxine sensitivity.

What all the above examples of epigenetically
determined evolutionary changes have in common
is the fact that signal cascades that lead to
induction/loss of these evolutionary phenotypic
changes start in the CNS. This suggests that the
epigenetic information for these evolutionary
changes comes from the nervous system and not
any other organ, organ system or part of the body.

Before I discuss the origin and the nature of this
epigenetic information, in the next post I will
present additional evidence on the neural
control of individual development.

N.C.

.

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