evolution and ontogeny Flashcards
ontogeny definition
The complete developmental trajectory from egg to adult, and in many organisms the process is ‘indirect’, including separate larval and adult stage
ontogeny timeline: Maria Sibylla Merian (1647 – 1717)
A German naturalist
One of the earliest scientists to work on the development of insects and metamorphosis from larvae into the adult stage
Her work describing the stages of development from egg to larva to pupa and then the transformation into the adult
Her work dispelled the (then popular) notion of ’spontaneous generation’.
It was early work documenting the ontogenic life cycle (though term coined later).
ontogeny timeline: Charles Darwin 1809-1882
Recognised the need to understand ‘heritable variation,’ both the mechanism of inheritance and the developmental process by which phenotype was generated.
Theorised that both adults and earlier life stages could be subject to natural selection.
Attempted to explain inheritance with his theory of ‘pangenesis’ in his book ‘the variation of animals and plants under domestication’
His theory was wrong
He proposed that ‘gemmules’ - minute particles of inheritance thrown off by all cells, modified by an organism’s environment, congregate in reproductive organs of parents to be passed on to their offspring.
see Fairbanks (2020) https://doi.org/10.1038/s41437-019-0289-9
ontogeny timeline:
Karl Ernst von Baer (1792-1876)
Ernst Haeckel (1834-1919)
D’Arcy Thompson (1860-1948)
Karl Ernst von Baer (1792-1876)
-An embryologist known as the father of embryology
-came up with ‘laws of divergence’
-First law: “the general features of a large group of animals appear earlier in the embryo than the special features”
Ernst Haeckel (1834-1919)
- Another embryologist
- came up with the ‘biogenic law’ that ‘ontogeny is a recapitulation of phylogeny’
- http://www.kuriositas.com/2012/01/art-forms-of-nature-ernst-haeckel.html
D’Arcy Thompson (1860-1948)
- proposed a theory of ‘transformations’
- whereby morphological characters evolved as co-ordinated changes in body form – allometric patterns during the later stages of ontogeny
ontogeny timeline:
Richard Goldschmidt (1878-1958)
Gavin de Beer (1899-1972)
Homeobox genes discovery (1983)
Richard Goldschmidt (1878-1958)
- studied homeotic mutations in Drosophila
- He used this study to develop his theory for – ‘saltational’ evolution (‘hopeful monsters’).
- Theory was generally dismissed due to the assumption that extreme forms wouldn’t find mates
- However others could see merit in his theory
(see Theissen 2009 Theory Biosci. 128, 43-51)
Gavin de Beer (1899-1972)
- worked on the implications of evolutionary changes in the timing of developmental events – ‘heterochrony’.
Homeobox genes discovery (1983)
- The birth of Evo-Devo came with the discovery of homeobox genes by two labs independently in 1983
- Ernst Hafen et al. at the University of Basel
and Mathew Scott et al. at Indiana University
- This discovery provided a molecular basis for homeotic mutations, and a better understanding of the process of developmental re-patterning.
Developmental re-patterning 4 effects and their definitions
This provides a framework for the evolution of new phenotypes whereby the ‘developmental trajectory’ provides the raw material on which natural selection can act.
Mutations that change developmental processes have one or more of the following four effects:
Heterochrony – changes in the relative timing of developmental processes of descendents compared to ancestors
Heterotopy – changes in the relative spatial positioning of developmental processes
Heterometry – changes in the relative sizes of parts of an organism, or in the relative concentrations of gene products
Heterotypy – the evolution of new types of structures.
Cellular activity during development is genetically controlled, and includes 4 key processes:
1) Cells divide and proliferate – the rate, plane and duration of proliferation need to be controlled to generate the specific adult form.
2) Cells differentiate (stem cells) – there are over 200 cell types in the adult, which start from very similar cells early on. Each cell has the same genome, so differentiation is about the differential switching on and off of genes
3) Cells move – this is an especially important feature of gastrulation in animals, when cells stream from one part of the embryo to another. Movement can be induced by trans-membrane proteins among other processes.
4) Cells die – programmed cell death is known as apoptosis, and is a necessary part of development where some cell types need to have a shorter lifespan (e.g. epithelial cells) than others.
Changes in one of these four processes (or some combination) could result in heterochrony, heterotopy, heterometry or heterotypy
Heterochromy
One way a change in the timing of development can impact on the phenotype of the adult form is by having the adult form retain characteristics previously only seen in juveniles
This is called paedomorphosis - ‘neoteny’ (slower development) and ‘progenesis’ (earlier sexual maturation) are both versions of this.
Heterochrony can be promoted at a molecular level in various ways
Example paper: rapid radiation of species an African Cichlid fish study
- In this study the expression of genes governing light perception (opsin genes) was studied in cichlids by Carleton and co-workers
- 3 pigment sets were studied: UV, violet and blue
(http://cichlid.umd.edu/cichlidlabs/kc/res/vision.html)
Example paper: Carleton et al (2008 BMC Biology, 6:22) comparing various species of Fish
- Some were ‘direct developing’ I.e. showed the adult expression pattern from an early age and showed the typical increase of expression over time
- Others showed continued low expression from early developmental stages (neoteny)
- Comparing species, different expression patterns corresponded to different habitats
Heterotopy example: flatfish
Example: the case of the flatfish (Order Pleuronectiformes):
The external features of adult vertebrates are typically symmetrical, and this is true of the other 39 Orders of Teleost fish.
The larval stage of a flatfish is symmetrical like its ancestors, making this look like a case of ‘recapitulation’ (when ontogeny repeats phylogeny), but may simply reflect a later stage modification of the developmental process.
In flatfish the eyes migrate from symmetrical alignment in larvae to asymmetrical alignment on adult fish where both eyes sit on top of the head
Are the ~500 species of flatfish the descendants of a ‘hopeful monster’ event ~65M years ago? The discovery of intermediate forms from the Eocene (~50Ma) by Friedman (2008, Nature, 454, 209-212) suggest instead a gradual evolution – see Friedmans illustrations.
The molecular mechanism for eye migration is not yet fully worked out, but likely involves timing of hormone production from the thyroid
See: Tagawa & Aritaki 2005, Gen & Comp. Ent. 141, 184-189
Thyroid hormonal changes during development affected colour (A vs B) and body symmetry
Another heterotopy example: fang position in snakes
In an example involving the anterior – posterior axis, the position of fangs in snakes appears to have evolved from an ancestor with no fangs, to one with rear fangs, to the most recent with front fangs, evolving independently within the lineage at least twice (Vonk et al. 2008, Nature, 454, 630-633)
The development of the fangs is controlled by expression of ‘sonic hedgehog’, one of three types of hedgehog loci in vertebrates.
For the ancestral forms (no fangs and rear fangs) expression of this gene is along the extent of the upper jaw (a & c in figure), while in the front fanged species (b, d & e) expression is localised in the posterior part of the jaw (but not in the anterior part where the fangs will form).
The fangs are then displaced to the front during ontogeny (consistent with the rear fang ancestral origin).
An example of heterotopy and heterometry occuring together:
development of longitudinal crest in voles and mice
Jernvall et al. (2000, PNAS, 97, 14,444-14,448)
heterotopy involving a shift in the orientation of dental cusps from alternating in the ancestor and in the modern vole, and parallel in the mouse
heterometry involving an increase in the number of cusps in the vole.
Sonic hedgehog (shh) again plays an important role, showing a shift in the orientation of expression in the vole as development progresses
Another heteroropy and heterometry example
development in frogs
(Yanai et al. 2011 Dev. Cell 20, 483-496)
this study compared the expression profiles of a number of relevant genes during development for two congeneric frog species (frogs of the same genus)
the profiles match very well for many genes
but in some cases the amount produced is greater for X. tropicalis.
Heterometry observed in the ‘complement system’ genes
Heterochrony shown in hatching enzyme
X. tropicalis hatching genes tending to be induced earlier and decrease sooner.
Heterometry example:
Eye loss in the cave races of the fish Astyanax mexicanus, gene expression and the loss of the eyes
( Retaux et al. 2008 Biol. Cell 100, 139-147)
At 10-12 hours post fertilisation (hpf) shh (sonic hedgehog) signalling along the midline (green) is greater for the cavefish, and the eyefield deliniation by Pax6 expression is reduced (purple)
At 24 hpf lens apoptosis starts in the cavefish – so the eye forms, and is then removed
In the adult fish the eye is completely regressed in the cavefish/ fully developed in the surface fish
Some issues raised by the Cavefish eye example
Why build an eye if you’re then going to remove it (seems expensive)?
The answer may be that normal fore-brain development requires the concomitant production of eyes, since the cells for each intermingle from early stages.
Why remove the eye at all – can’t see in the cave, but why loose the eye?
One possibility is ‘antagonistic pleiotropy’. This is where the same genes that enhance some features also reduce others. It isn’t known if this is relevant in this case, but has been demonstrated for other traits
Heterometry can be positive or negative. In this example, both occur.
While the eye is being lost, other traits (e.g. taste buds) are being increased. Note that with heterometry, there is also often necessary heterotopy to compensate, possibly associated with heterochrony (see Arthur chapter 10 for further discussion).
Heterotypy definition
the evolution of novel forms or appendages
e.g. poisonous claws in the centipedes.
HOX geneexpression is unique for this segment of the body. Capacity evolved relatively early in the broader lineage, and was then lost again in descendent lineages .
HOX gene expression is unique for this segment of the body. Capacity evolved relatively early in the broader lineage, and was then lost again in descendent lineages.
e.g. transition of form and strategy (Fabrezi et al. EvoDevo (2016) 7:5)
- Frogs that extrude their tongue to catch prey (anuran non-pipoids)
- Frogs that bite and extrude their tongues (ceratophyrids)
- Lepidobatrachus frogs evolved to hunt underwater losing the tongue extrusion habit
