Was Darwin Wrong?

[Update: I understand that the cover of New Scientist says "Darwin was wrong" and as Bjorn has just told me, this is the original article. I'll read that one as soon as I can.]


A new article in the Guardian (hat tip Bjorn at Pleion) has the headline :

Evolution: Charles Darwin was wrong about the tree of life


I think this headline, and the spin of the article in general is a rather extreme over-simplification, and more importantly, it is subject to misinterpretation by anti-evolutionists.

The main points I want to make are:

1. It is an oversimplification to say that Darwin was "wrong" on this point. It is not a clear cut case of right or wrong. Instead, the facts as we understand them today are more complex than what Darwin envisioned, or could have envisioned (given he didn't know about DNA).

2. The primary, most general implication for the history of life is not changed. Darwin's tree of life posits common ancestry of all life. This is the central scientific fact that anti-evolutionists rebel most against (because they don't want to admit we are all related to slime-molds, etc). In fact, the new observations about biology continue to reinforce Darwin's history-changing insight that all life shares a common ancestry. Yes, we share a common ancestor with a chimp and a fungus, get over it.


Below is what I wrote about our changed view of the Tree of Life in a paper with Michael Rose, published here in the Open Access journal Biology Direct.

Complications for "The Tree of Life"

Nineteenth and 20^th Century biologists generally conceived of a "Tree of Life" – a mostly bifurcating graph connecting species in an order that reflects their common ancestry. At least three processes complicate such a view of a tree of life, horizontal transfer, symbiogenesis, and differential lineage sorting of genes. Each of these processes are at odds with fundamental assumptions of the Modern Synthesis [7,8] and a Tree of Life for the new biology is necessarily more complex than a graph joining species.

In the middle part of the 20^th Century, it was often supposed that organisms and their cells are sleekly functional (Fig. 2A). Given such assumptions, passing genes from one species to another would not be favorable if those genes were finely tuned for the necessary functions of the species from which they originate. Even the movement of genes within a single genome was not accepted by the biological mainstream at that time, despite McClintock's early discovery of accessory elements in maize [9]. Nevertheless, molecular characterization of transposable elements in the late 1970s finally undermined the view of the genome as a static, well-organized library of genetic information [reviewed in [10]]. With the advent of genome sequence data, researchers studying the molecular phylogenetics of bacteria realized how common prokaryotic horizontal transfer is [11,12].

Similarly, modernist preconceptions led some to discount the importance of endosymbioses in the origins of new life forms, like eukaryotes. Broad theories of endosymbiotic origins for species had been suggested in the late 19^th and early 20^th Centuries [7], but were ignored save for a few well-established cases like lichens. By the 1980s, the evidence for symbiogenesis in major cell biological events was voluminous [13,14].

Even systematics has had to abandon many strictures that were part of the Modern Synthesis. If species are the durable unit of biology, and if natural selection quickly molds genes to current utility, then most genes should diverge at the time of speciation events, given views like Mayr's. Here again, analyses of newly abundant sequence data in the late 20^th Century showed that rather than a highly congruent coalescence of genes at the times of speciation events, the coalescence times of alleles among species are highly variable. As such, species trees and gene trees often cannot be equated [15,16].

These phenomena complicate the tree of life. Rather than a graph connecting species, the tree of life itself is hierarchical: A universal tree of species is largely a human-imposed ideal because the components of any particular species have evolutionary histories that are not congruent with each other. This incongruence has a clear and well documented mechanistic basis in horizontal transfer, symbiogenesis and differential lineage sorting (not to mention gene duplication explained above). These processes together undermine the existence of a tree of life defined only at the level of species, pointing instead to branching histories that often differ among levels of organization and scales of analysis.

Figure 2. Old and new views of the evolution of prokaryote genomes. (A) 20^th Century biologists sometimes assumed a close congruence between gene history and species history. Horizontal gene transfer was assumed to be uncommon, as the process of genes entering a new genome is counter to the idea of a sleek and well adapted genome. (B) After analyzing the genomes of many prokaryotes, biologists recognized that horizontal gene transfer may be a common event. Furthermore, prokaryote species trees may be viewed as a patchwork of gene trees with varying levels of congruence. A similarly hierarchical view of eukaryote evolution has been articulated by Maddison [15], except that differential coalescent times – usually not horizontal transfer – is the primary mechanism used to explain incongruence of gene and species trees.

And in the response to reviews:

2. Rose and Oakley bring up the newly apparent prevalence of horizontal gene transfer as one of the major blows to the 20^th century perspective in biology. This is, certainly, true, but I think the discussion in the paper stops short of really driving the nail down. The real issue is that, when fully conceptualized, extensive HGT undermines the very notion of the Tree of Life (the TOL paradigm) which, certainly, is a big part of the Modern Synthesis (as well as the classical, Darwinian foundation of biology). Simply put, although trees are crucial in depicting certain phases and aspects of life's history, there is no TOL as such, i.e, evolution of life cannot be presented as a tree, so Darwin's famous simile fails as an overarching generalization. The demise of the TOL paradigm is covered in several recent papers [91,92]. Again, this is related to the problem of "eukaryotic chauvinism": the tree pattern might hold for the evolution of the major divisions of eukaryotes (although not necessarily for all eukaryotes taken together) but, certainly, not for prokaryotes, let alone the entire history of life.

Authors response – Here we disagree with Dr. Koonin. HGT does not necessarily undermine Darwin's "Tree of Life" completely, even though in post-Modernist biology this Tree of Life is much more complex. Today's Tree of Life, as Dr. Koonin points out, is different from what Darwin envisaged, in that it is multi-dimensional – branching histories characterize in a complex way multiple levels of organization, not just the species level. Further, as discussed in the article, HGT is not the only blow to a two-dimensional tree; paralogy, endosymbiosis and lineage sorting also contribute to a new, highly multi-dimensional view of evolutionary history.

This emerging understanding of the trees of life is pluralistic, encompassing the branching history of biological units at all different levels of organization [81]. The evolutionary histories of units at different levels (gene domains, genes, species, etc) are not always congruent with each other, yet there are still branching histories that characterize each of these levels. Branching history is a pattern that results from well known mechanisms including exon shuffling, gene duplication, genome duplication (polyploidy), co-option, speciation, and vicariance of multiple species. HGT is one example of a mechanism that causes branching histories at different levels of organization to be incongruent. It clearly points out the failed assumption that the history of components is congruent with the history of the higher level unit to which it belongs. Nevertheless, this assumption can be used as a valuable null model to understand macroevolutionary patterns and processes [93]. As we discussed in this article, the species was usually seen as the durable unit driving branching at all levels, but the existence of multiple evolutionary levels and mechanisms violates this assumption.

Processes to split biological units pervade all levels of the biological hierarchy. Protein domains duplicate within genomes and may be "horizontally transferred" from one gene to another. Genes may form units of synteny or operons, but individual genes may also be copied from one part of the genome to another or from one genome to another, independently of the rest of a synteny unit or operon. Whole chromosomes and whole genomes may also duplicate by various mechanisms. All these processes create the new tree of life. But that tree is a postmodern tree, rich in complexity. Components coalesce to form units with a congruent path for a time, only to be broken up. There is no reason to provide anti-intellectual, anti-evolutionists with quotes like "The Darwinian paradigm is dead", because this complexity only enhances Darwin's most profound insight – the universal common ancestry of life.