Evolutionary coverstories

Great things are not done by impulse, but by a series of small things brought together.

Vincent van Gogh

People have long suspected that the first organisms must have been relatively simple. Since the origin of life, some organisms must therefore have undergone important evolutionary transitions that resulted in the kinds of species with which we are now familiar. In recent years,biologists have come to view these transitions not only as revolutions in the way living organisms looked and behaved, but also as solutions to similar problems. Understanding how they occurred brings us great insight into how natural selection works, and why modern, complex, organisms live and behave as they do.

Two people, John Maynard Smith and Eors Szathmary, did much to promote this conceptual unification in the 1990s (Szathmary and Maynard Smith 1995; Maynard Smith and Szathmary 1995, 1999). Together they defined eight major transitions (Figure 2.1), united by changes in the way that genetic information is transmitted between generations. In the origins of life they postulated individual replicating molecules forming populations of such molecules in compartments, such as cells (1). Later on these replicators bound physically together into chromosomes (2). Eventually, RNA, acting as both a replicator and metabolic catalyst, largely gave up these functions to more specialist molecules: DNA and proteins (3). Some prokaryotes (bacteria) eventually transformed into eukaryotes (4). Asexual clones among the eukaryotes transformed into sexual populations (5). Some single-celled protists transformed into multicellular organisms (plants, animals, and fungi) (6). In a few groups, solitary individuals began to live in social colonies (7), and in one of these, our own species, language emerged (8). We therefore bear the distinction of being the only lineage that has undergone all eight transitions. This would make us, in some quantifiable sense, the most complex biological entities not only in what we have evolved but in how we evolve.

Explaining these individual transitions is challenging for three reasons, summed up by three different senses in which they are 'major'. The first, and the one that Maynard Smith and Szathmary stress, is in an intellectual sense; the phenotypic changes we have to postulate are in themselves changes to the genetic system. This requires us to think especially hard about how evolution works because evolutionary biologists normally have the luxury of assuming that the genetic system is a constant. The second use of the word 'major' is in a structural sense: that the phenotypic changes were large. However, to be consistent with Darwinian evolution, changes must proceed by a series of small steps that retain functional integrity and which will be favoured by selection in each generation. We must first therefore imagine possible intermediate phenotypes, not all of which might be illustrated in the world about us.Then we must imagine environments or circumstances in which all the postulated intermediates would be favoured. In meeting these first two challenges we are postulating solely the origins of the characters involved. The third meaning of the word 'major', however, is that the changes were in some sense 'successful' from a macro-evolutionary perspective. In this sense we are implying that the transition was retained to the present day, and usually retained in abundance. This creates special challenges because, as will be shown later, the transitions can be seen to set up potential conflicts that would disrupt the integrity of the new system. Many of the transitions require formerly independent, or even totally new, genetic systems to come together and cooperate as part of a larger system. Yet, biologists are now used to the idea of genetic entities displaying selfish behaviour to ensure their own persistence. Thus it is sometimes problematic to imagine persistence of the novel unit. To cap off our problems, hypotheses must be consistent with existing evidence. Thin though that often is, even a little evidence can establish useful boundaries to possibilities, as fictional detectives are apt to explain.

In the third sense, the transitions were not initially major, but with the benefit of hindsight, having stood the test of time, many can now be seen to be so. To be retained in abundance, there are four possible contributing processes. First the transition might have happened on numerous occasions. In fact this is normally not the case. All of the transitions have happened to our knowledge only once, with the exception of multicellularity and social colonies, which have both evolved a limited number of times. This relative uniqueness is unsurprising given the drastic nature of the changes. The other three processes are; (1) reversal to the ancestral state, which might have been limited; (2) extinction of clades possessing the trait, which might have been reduced; and (3) speciation of clades possessing the trait, which might have been increased. The problem with explaining persistence is to find evidence for or against these processes.

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