Books : reviews

Wallace Arthur.
The Origin of Animal Body Plans: a study in evolutionary developmental biology.
CUP. 1997

Wallace Arthur.
Biased Embryos and Evolution.
CUP. 2004

rating : 3.5 : worth reading
review : 2 November 2010

This is a nice book in the "evo-devo" discussion. Arthur argues that development is a first class partner in the evolutionary process. To understand evolution, we have to understand how it acts over the entire lifecycle of the organism, not just its adult phase (since organisms have to be "fit" at all stages of their development, and since the majority of organisms are selected against -- die -- before adulthood).

p1. all organisms are four-dimensional things. … organisms do not have life cycles, rather they are life cycles. We tend to picture adults …

p2. Every stage in a life cycle only comes into being if the previous one survives. … at the level of the population there will be natural selection at every stage

p3. most species experience most mortality at young rather than old ages

p31. If a character does not emerge until late in a life cycle, it will be invisible to natural selection for all those early stages during which much mortality occurs.

Understanding how the process acts throughout the lifecycle means we have to incorporate the effect of development as well.

p37. the [modern] synthesis focused too much on destruction and the external environment and not enough on creation and internal coadaptation.

But it is not sufficient merely to "bolt on" a bit of development to the theory. The development process contributes an intimately intertwined developmental bias aspect to the overall process.

p38. mutation and development are both important determinants, alongside natural selection, of the directions that evolution takes. … it is the interactions between them that are crucial, rather than one of them acting in isolation.

p51. the way in which genes and signalling molecules interact … constitute the 'chemistry' of development. But development also has a 'physics' … developmental processes are systems with quantitative dynamics.

Development is an inherently dynamic process, carving out a trajectory through character space.

p52. The only way that natural selection can make new kinds of adult is by altering the course of development. And it can only make use of the variations that it finds at each stage of the life cycle. So some things can be modified in early development, others not until later.

p74. development has a much more far-reaching effect in determining the direction of evolutionary change than merely closing off a few avenues. I believe that it does this in two main ways, one concerning the structure of developmental variation … and one concerning the developmental system's integration as being itself a target of selection

Not only is development dynamic, it is fast:

p199. evolution ... has created organisms with trillions of cells from a single-cell starting point over a period of about a billion years. [Development] repeatedly achieves the same thing over a single lifetime.

Arthur points out that we have terms for certain evolutionary processes, but not for this developmental, organismic level process.

p81. What process causes the appearance of novelty at the genic level? Answer: mutation. What process causes the appearance of novelty at the whole-population level? Answer: natural selection. But what process causes the appearance of novelty at the organismic level?

So he coins a new term: 'developmental reprogramming', to refer to this process. He identifies four kinds of changes that can be made to the developmental programming (noting that there are, of course, intertwined connections between different changes at different stages):

p83. At the developmental level, novelties can be initiated in any of four ways: by altered timing, positioning, amount or type of gene product. ... However … there are many steps in the developmental process … the nature of the change may alter as development proceeds.

Development itself is intertwined with other levels of evolutionary process:

p85. Development will only be reprogrammed in a heritable way if a gene has mutated.

But this developmental aspect of evolution, Arthur argues, has received short shrift in the standard theory.

pp86-7. So, evolution works as follows: genes alter by mutation; development alters by reprogramming; populations alter through selection (and drift); new species arise when populations diverge to the point where they become reproductively isolated. Mutation, selection and reproductive isolation are already well represented in evolutionary theory. Reprogramming is not.

The reason that it needs to be incorporated is that it results in an inherent bias to the evolutionary process that cannot be explained or understood if development is not considered. Different developmental trajectories may be easier to reach than others, leading to developmental bias (p201. the tendency of the developmental system of any creature to produce variant trajectories in some directions more readily than others).

p115. some forms of reprogramming can be produced by many mutations, while others are produced by only a few. That is, some changes are 'easier' to achieve than others. So even if the rates of occurrence of different mutations at the molecular level are equal (and usually they won't be), the result will be a higher probability of producing some mutant individuals than others

This is clear even if we think of a non-linear genotype-phenotype mapping. Selection acts on phenotypes; given a non-linear mapping some of these will be more readily obtainable from small mutations than others. Add to this, as Arthur does, the fact that selection is occurring during the process of this mapping unfolding (ie, over the whole developmental life-cycle of the organism), and that the developmental process itself is heritable and mutable, it is certain that things are much more complex than just mutating genes.

p130. one way to picture an embryo is as a trajectory through multicharacter hyperspace. ... Characters that were not there initially gradually come into being. We go from no brain to proto-brain to small brain to bigger brain.

p151. phenotypic plasticity should not just be thrown out of the window by evolutionary theorists because it is not inherited. If you take one step back from the non-inheritance of 'plastic' variants, you will probably find that the pattern of plasticity is itself inherited, or at least partly so, and that there is variation for it in a 'typical' population.

p195. Reprogramming is a more complex process than mutation, because it is a change in something that is itself by definition a state of change. Development is a trajectory through multicharacter hyperspace; developmental reprogramming is a mutationally induced change in that trajectory.

One feature of developmental reprogramming is "duplication and divergence". A stage or module that occurs once can, with a relatively small developmental change, occur more than once. The new occurrences can then diverge, be modified independently, without compromising the functionality of the original.

pp153-4. what particular features of organismic design increase the probability that evolution will find a way to produce advantageous modifications?
     ... 'modularity' ... 'duplication and divergence'

This "duplication and divergence" is a pattern widely seen in development, possibly nowhere as obviously as in segmented body plans, where instances of duplication can be accompanied by wild diversification, yet sometimes by very little.

p155. an arthropod needs a minimum of two pairs of legs for stable land locomotion … all the vast array of arthropods have more than this: three pairs of legs in insects, four in arachnids, 'many' in crustaceans and 'very many indeed' (sometimes more than 100) in the appropriately named myriapods. Given that there is an excess of legs over what is required for locomotion, surely some could be modified into other things? Well, yes, and there are lots of cases where this has clearly happened. Many arthropod mouthparts are smallish paired appendages that have been derived from 'spare' pairs of legs in an ancestor. The centipede's impressive poison claws … have probably also been derived in this way.
     However … we have not yet developed any predictive ability. Centipedes, for example, would appear to have a particular surplus of legs, and yet the 'longest' ones, with 191 pairs, have not specialized any more of them into other things than the shortest, which have only fifteen pairs.

This examination of centipedes is followed up by an intriguing observation of a clear bias in their developmental program:

p206. does developmental bias exist in the real world…? … all known species of centipedes have odd numbers of leg-pairs (between 15 and 191). Not a single species has an even number. If there were only three species of centipede, we could write this off as being due to chance; but since there are in fact about 3000 species, this explanation is clearly untenable.

This is a lovely discussion of the evo-devo field, with a personal slant from the author who is deeply immersed in it himself. The idea of evolvable developmental programming resonates with me, as a computer scientist, because it provides a clear mechanism for higher level processes and modules to appear and be built on, without having to go back down to primitive components all the time. Once these higher level processes appear, and evolve, higher levels still can be built, and complexity can take off.