evolutionary theory

New Scientist has an article by Mark Buchanan discussing horizontal transfer as a mechanism for the evolution of early life: "Horizontal and vertical: The evolution of evolution"

There's a lot of "evolution doesn't work the way we thought" stuff in the article, which focuses on Carl Woese:

How could modern biology have gone so badly off track? According to Woese, it is a simple tale of scientific complacency. Evolutionary biology took its modern form in the early 20th century with the establishment of the genetic basis of inheritance: Mendel's genetics combined with Darwin's theory of evolution by natural selection. Biologists refer to this as the "modern synthesis", and it has been the basis for all subsequent developments in molecular biology and genetics. Woese believes that along the way biologists were seduced by their own success into thinking they had found the final truth about all evolution. "Biology built up a facade of mathematics around the juxtaposition of Mendelian genetics with Darwinism," he says. "And as a result it neglected to study the most important problem in science - the nature of the evolutionary process."

In particular, he argues, nothing in the modern synthesis explains the most fundamental steps in early life: how evolution could have produced the genetic code and the basic genetic machinery used by all organisms, especially the enzymes and structures involved in translating genetic information into proteins. Most biologists, following Francis Crick, simply supposed that these were uninformative "accidents of history". That was a big mistake, says Woese, who has made his academic reputation proving the point.

I don't see any inconsistency between the modern synthesis and the idea of horizontal gene transfer. This is a failure of history -- of people reading only Ernst Mayr as a representative of the synthetic view. Other voices -- especially Stebbins -- emphasized gene transfer. The dynamics of genes themselves, as opposed to genes as mere parts of organisms, surely underlie the next generations of evolutionary theoriests, including Dawkins' gene-centric perspective, and Williams' idea of "levels of selection".

Woese is working to discover modes of evolution of gene (and even sub-gene) replicators, before the "hardening" of genomes into organisms. Before the organismal level of selection existed, there can only have been the gene level (taking "gene" to mean replicating element). That's not anti-synthesis, it's what we would expect of replicators at the sub-organismal level.

It's also no surprise as applied to horizontal transfer in more recent lineages. Humans have gotten DNA from viruses during the past few million years, some of which has been fixed in the genomes of the present population. That's no challenge to the way we understand evolution, it's saying that one kind of mutational process is acquisition of viral DNA. Likewise, the introgression of genes between species is no challenge to evolution. It is good evidence that speciation is a evolutionary process -- otherwise boundaries between sister species would be impermeable.

Chapter 2 of R. A. Fisher's Genetical Theory of Natural Selection is remarkable for many reasons. In it, he presents a model of selection in an age-structured population, the concept of reproductive value, and the Fundamental Theorem. Toward the end of the chapter, he discusses "The Nature of Adaptation," presenting a geometric model to justify the assertion that the probability of favorable genetic changes declines as the effect size of those changes increases.

I'd like to point readers to a recent essay in Evolution, by Scott V. Edwards, titled, "Is a new and general theory of molecular systematics emerging?"

Edwards covers some of the recent progress and problems encountered when using molecular evidence to test phylogenetic hypotheses. A sampling of the issues: How do we combine information from different sets of molecular data? Can we just compile sequences from many gene loci together into one analysis ("concatenation"), or do we need to make allowances for genealogical diversity among loci? How do prior assumptions affect the outcomes of analyses, like the presence or absence of polytomies (branching points where three or more species emerge simultaneously)?

I try to think of things that students should read as they get up to speed with evolutionary genetics. Edwards' essay raises many important points, and as I read through it, I reflected on the ways that paleoanthropologists increasingly need to be aware of the inner workings of molecular studies of phylogeny.

If we're interested in the phylogeny of species, we need to know how the "tree" of relationships of species may be manifested in the genealogical relationships among genes. Discordances between genes result from the fact that gene trees are not species trees. Species are genetically variable, and the living descendants of an ancient species may have inherited different parts of the variation of ancient species. Depending on the demography of that ancient population, gene trees representing the evolution of two distinct genetic loci may have different topological properties.

From Edwards:

John Avise encapsulated the relationship between gene and species trees well in 1994: “Gene trees and species trees are equally “real” phenomena, merely reflecting different aspects of the same phylogenetic process. Thus, occasional discrepancies between the two need not be viewed with consternation as sources of “error” in phylogeny estimation. When a species tree is of primary interest, gene trees can assist in understanding the population demographies underlying the speciation process” (pp. 133 and 138 in Avise 1994). This essay is in part meant to reemphasize Avise' perspective and to remind readers that species trees are in fact the “primary interest” of systematics.

Genealogies involve some unknown parameters. Applying the fossil and archaeological record may let us constrain those parameters, just as applying molecular biology and pedigree comparisons may let us constrain the parameters describing the mutational process.

To my mind, this is where paleoanthropologists need to be most attentive: Molecular methods are not in conflict with fossil approaches, they implicitly depend upon them. Yet, communication between the two fields rarely involves actual numbers, so a frequent occurrence is that a "bottleneck" in paleoanthropology with a 10 percent reduction in population becomes a "bottleneck" in genetics with a 1000-fold reduction in population.

Testing of demographic hypotheses moved on to genome-wide polymorphism data several years ago. The logical equivalent for species divergences is lineage sorting -- a model that's been applied since the mid-1990's. The hominoids are extremely well studied from the standpoint of molecular systematics, and remain the central example in most theoretical papers incorporating multiple loci. This year I have noticed several interesting implementations of whole-genome polymorphism comparisons among species embedded in phylogenetic trees. The higher mutation rate of CpG sites has long been known, but we now know that a 50-bp or longer flanking region may influence local mutation rate. As we move from genes to gene networks, our comparisons will not be the same nucleotide, but classes of mutations across classes of genes.

This is another of those cases where the future lies in better algorithms. Edwards seems a man after my own heart -- the computer programs lend a superficial veneer of rigor, when the underlying assumptions are in need of challenge:

Producing phylogenies directly from gene sequences essentially in one step, without additional transformations, is now the dominant mode of phylogenetic analysis and indeed it has advanced the field enormously. Nonetheless, I suggest that the very success of this paradigm and the ease with which phylogenies could be produced directly from DNA matrices led to a comfort zone in phylogenetics. If we can imagine systematic methods themselves as a likelihood surface, I suggest that the current paradigm is a local optimum in that surface, an optimum that is useful but ultimately incomplete in so far as it has failed to model the potential for gene tree/species tree discordance even cursorily (Fig. 3) (Edwards 2009:6).

His theme is an old one -- how do we use "total evidence" methods in phylogenetics. Variance among loci gives the problem a newish twist, one that may add information that other techniques have left on the table. But we have to wring it out of the data.

References:

Edwards SV. 2009. Is a new and general theory of molecular systematics emerging? Evolution 63:1-19. doi:10.1111/j.1558-5646.2008.00549.x

I'd like to point readers to James Crow's article in the open access Journal of Biology. Titled, "Mayr, mathematics and the study of evolution," it's a brief summary of some of the important results from mathematical genetics -- sort of a follow-on to Haldane's "A defense of beanbag genetics".

Coming fifty years after Haldane's effort, Crow has been able to include a lot more stuff -- in particular the consequences of the mathematical development of neutral theory, and the effects of computers, permutation tests, and molecular clock models in phylogenetics.

I cannot help but quote this passage, which is direct:

Ironically, Mayr himself unwittingly provided an especially compelling argument for mathematical analysis. His theory of “genetic revolutions” assumed that from a well integrated population, genetic drift in a small founder offshoot will sometimes produce a population with a new set of genotypes integrated in a new way. Intuitively, a small founder population seemed a particularly unlikely place to find a new favorable gene combination, and this was indeed shown to be the case in a very detailed mathematical analysis by Barton and Charlesworth [5]. If Mayr had had more respect for mathematical population genetics, he never would have made what most theorists regard as the mistake of proposing that small founder populations are a likely source of major evolutionary changes by genetic drift (Crow 2009:13.2).

Lest you think this is an argument against the role of chance, Crow later describes the more au courant view of speciation:

Until recently, mathematical theory had contributed little to the study of speciation. Mayr emphasized allopatric speciation and the prevailing model, due to Dobzhansky and Muller [9], prevailed. Recent mathematical studies [10] support it and favor the view that speciation genes correspond to normal genes, selected for their effects within the species. Furthermore, there is evidence that these genes evolve rapidly. Thus, hybrid incompatibility is a by-product of ordinary selection in geographically isolated populations (Crow 2009:13.4).

This model of speciation recognizes chance and contingency, but not mainly from stochastic fluctuations in allele frequency (drift). Instead we have the stochastic processes of mutation and environmental change and the (possibly complex) epistatic interactions among selected alleles.

There's more in the essay. Crow does refer to human evolution -- the out of Africa scenario and Neandertal genetics make appearances not entirely to my taste, but he notes that selective sweeps -- dear to my heart -- are an important feature of the recent landscape of mathematical genetics as well.

Crow could have included a number of other mathematical developments, particularly the Price equation, Hamilton's contributions, and Maynard Smith's "evolutionarily stable strategies", all of which share his theme of the mathematical derivation coming first, and the non-mathematical descriptive formulations only coming later.

References:

Crow JF. 2009. Mayr, mathematics and the study of evolution. J Biol 8:13. doi:10.1186/jbiol117

I went looking for Lowie, because I was curious about the introduction of the diffusion concept into cultural anthropology. The mathematical description of diffusion, originally developed in thermodynamics, became important in statistical genetics during the first half of the twentieth century. In particular, R. A. Fisher introduced diffusion methods to examine the effects of natural selection in his 1922 paper, "On the dominance ratio." Diffusion methods made it possible to derive analytical approximations for many interesting biological parameters, and also came to underlie models of population dynamics outside the field of genetics.

So I wondered: How did the use of diffusion in cultural anthropology compare to the introduction of the diffusion concept in genetics? Kroeber's systematization of the concept of cultural diffusion was certainly later than Fisher and Wright's major works on diffusion theory.

It turns out that "diffusion" was initiated into cultural anthropology by E. B. Tylor himself. The OED has the earliest anthropological use of the term in Primitive Culture:

How good a working analogy there really is between the diffusion of plants and animals and the diffusion of civilization, comes well into view when we notice how far the same causes have produced both at once.

Later, Boas also makes extensive use of the concept of diffusion, in essentially the modern sense as an alternative explanation to independent invention for a cultural trait. For example, in his 1891 article, "Dissemination of tales among the natives of North America," he compares the transfer of myths and stories among groups in the New World to that in the Old. He writes:

Then, we may ask, is there no criterion which we may use for deciding the question whether a tale is of independent origin, or whether its occurrence at a certain place is due to diffusion? I believe we may safely assume that, wherever a story which consists of the same combination of several elements is found in two regions, we must conclude that its occurrence in both is due to diffusion. The more complex the story is, which the countries under consideration have in common, the more this conclusion will be justified (Boas 1891:13-14).

So by the time Lowie was writing his Culture and Ethnology, the concept of cultural diffusion was well-established, and the Boasian school was concerned with classifying culture similarity in terms of diffusion.

Cultural problems tended to involve the spread of relatively large quantities of information -- reflected by the Boas quote above and its concern with the "combination of several elements." We can interpret this focus as a statistical consequence of observing culture: With so many potential observations, diffusion is difficult to distinguish from the null hypothesis of parallel development (chance similarity) unless the similarities are sufficiently detailed (involve a threshold of information) to prove otherwise.

I have not yet found anywhere that this concept of assessing diffusion by "information content" was formalized beyond verbal descriptions like Boas' above. I will review Kroeber's contribution later; he does not provide any formalism at all.

What I want to point out here is that this concept of diffusion is delimited quite differently from the use of diffusion models in genetics. Fisher and Wright initially introduced diffusion methods to deal with the effects of random changes of gene frequencies. In the case of Boasian cultural diffusion, random change will almost always fall short of the information content necessary to identify specific resemblances in a cross-cultural context.

I can imagine datasets on cultural traits that would be sufficient to test the hypothesis of undirected (non-selected) diffusion. For example, phonological data on dialects is often detailed and coded to geographic locations. If we approached these data with a diffusion model, they would in many cases be sufficient to demonstrate departures from the null model of undirected diffusion.

But most observations from ethnography are not of this character. For this reason, cultural diffusion is a priori a phenomenon involving direction by some selective mechanism. In genetics, this would be natural selection. In cultural variation, the selective mechanism may be less clear -- some combination of conscious decision, customs concerning borrowed behaviors, and functional efficacy may be involved.

In the case of natural selection driving a gene substitution through space, Fisher's model of a wave of diffusion assumed only a single parameter determining intrinsic increase -- the "reaction" term in a reaction-diffusion equation. This was sufficient because the only relevant difference between the selected and non-selected alleles was fitness.

The case of cultural diffusion, in contrast, makes it tempting to suggest that there might be many independent terms contributing to the spatial dispersion of a cultural trait. Traits might be different in that some are more transmissible than others; thereby spreading more widely. Some might have greater functional advantages than others. Some ideas might be impeded because they conflict with widespread taboos; others might be facilitated by the same factors.

I write all this because I'm curious about why there was not a more formal development of diffusion in the context of cultural theory. There was every potential of it: Boas did not begin with a formalization, but the ideas critical to a formal theory are present in his description. But the development of the field quickly went in the opposite direction -- away from formalization and toward description. This was despite the fact that the concept of diffusion became incredibly important in the conflict between the Boasian school of ethnology and the cultural evolutionism of Leslie White and others.

Others (non-anthropologists) did develop more formal theory, but this had little (if any) impact within anthropology. As I continue, I'll go back to the early cultural evolutionists Tylor and Morgan, and trace their influence on 20th century neo-evolutionists. Additionally, no account of cultural diffusion can omit the importance of the Kulturkreis school and its concept of the culture area.

I picked up a copy of Julian Huxley's Evolution: The Modern Synthesis this week at a book sale. It's funny -- the book was a review copy and bears the following bookplate:

To The Literary Editor:

Direct quotation in reviews is limited to 500 words or less unless special permission is given.

Well, I hope that the statute of limitations on the bookplate has passed, because I'm going to quote a lot more than 500 words out of this over the next few weeks.

I'll start with a passage from the first chapter. It brings to mind Mayr's famous comment about "bean bag genetics," but I find Huxley's approach at once more sympathetic and insightful about the nature of inheritance opposed to the way scientists describe inheritance:

In the early days of Mendelian research, phrases such as "in fowls, the character rose-comb is inherited as a Mendelian dominant" were current. So long as such phrases are recognized as mere convenient shorthand, they are harmless; but when they are taken to imply the actual genetic transmission of the characters, they are wholly incorrect.

Even as shorthand, they may mislead. To say that rose-comb is inherited as a dominant, even if we know that we mean the genetic factor for rose-comb, is likely to lead to what I may call the one-to-one or billiard-ball view of genetics. There are assumed to be a large number of characters in the organism, each one represented in a more or less invariable way by a particular factor or gene, or a combination of a few factors. This crude particulate view is a mere restatement of the preformation theory of development: granted the rose-comb factor, the rose-comb character, nice and clear-cut, will always appear. The rose-comb factor, it is true, is not regarded as a sub-microscopic replica of the actual rose-comb, but is taken to represent it by some form of unanalysed but inevitable correspondence.

The fallacy in this view is again revealed by the use of the difference method. In asserting that rose-comb is a dominant character, we are merely stating in a too abbreviated form the results of experiments to determine what constitutes the difference between fowls with rose-combs and fowls with single combs. In reality what is inherited as a Mendelian dominant is the gene in the rose-combed stock which differentiates it from the single-combed stock: we have no right to assert anything more as a result of our experiments than the existence of such a differential factor (Huxley 1943:19).

I try to emphasize this point whenever I introduce genetics: we know about inheritance because of our observations on organisms, not because we have traced the molecular effects of every gene. As when we interpret sounds into language, we depend on contrasts to see the effects of alleles. I am always amazed when we learn something new about these molecular mechanisms underlying observable phenotypes, because they manifest in so many different ways.

P. S. Yes, after all that, you deserve a picture of a rose-comb. But although Flickr has many, all are copyrighted, none Creative Commons. So, I won't republish, but here's a link to my favorite.