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.

There once was a man named Chuck

I decided to write a quick Darwin Limerick, inspired by the contest over at Dispersal of Darwin, and by the concepts of pluralistic Darwinism and common descent:

There once was a man from Down House
Who convinced me I'm cousin to a brown mouse
I'm glad as can be
That all life is a tree
Toe fungus to red grouse to crown louse

I'm still working on "There once was a man named Chuck"

Darwin in WSJ

I was waiting to meet with a banker today to wire money to Europe, and I picked up the Wall Street Journal. In it, I was surprised to find a book review of Darwin's Voyage of the Beagle. They have a section reviewing classic books, "masterpieces". Embarrassingly, I've never read this Darwin classic, I think I'll take it on my vacation. The review was short and readable, reminding us that young Darwin was a passionate naturalist and geologist. The review also makes a connection with today, pointing out how invasive species and extinction have dramatically changed the planet in the geological blink since Darwin's voyage. I especially liked the illustration of a youthful, vibrant Darwin in the Galapagos.

Coming to grips with common descent

Talk about a bump. Since PZ mentioned this blog, visits are through the roof. I'm not sure I really ever intended to blog for the masses; I was just using a blog as a motivator to write more often, and to collect ideas for a book that I am very slowly writing. But I feel a bit obliged to have something of substance, since so many intelligent people are spending time looking at these pages.

Since I am swamped finishing up our quarter, and preparing for a family vacation to Europe, I'll pull something off my hard drive, which is pretty good. Here is a little set up: Only the most irrational and fundamental creationists object to natural selection, or "microevolution". The real barrier to the acceptance of evolution is recognizing global common descent ("macroevolution"), and especially the inference that humans are not specially created, but a twig in the tree of life. At the same time, natural selection is often directly equated with Darwinism (see this post for example) and evolution itself. I'm very slowly working on a book that explores the implications of common descent (pattern) and the processes that produce it (speciation, gene duplication, and "duplication" of biological units in between genes and species, like gene networks and traits). This post is an excerpt from a draft of one chapter. I've edited it down a bit, but it's perhaps still a little long and technical for a blog post - but pharyngulites are a smart bunch, so I have faith. For what it's worth:



Coming to grips with common descent

One of the most profound insights in the history of human thought is Darwin’s proposal that all species are united by common descent. The idea transformed the view of humankind’s place in the natural world from a self-congratulatory perch atop the Scalae Naturae to an arbitrary outpost alongside other apes as cousins to every palm, gastrotrich, and canary (note the goal here was to rhyme names of organisms with "Tom Dick and Harry", the colloquialism meaning "everyone"; not sure if anyone ever gets that though). We are still coming to grips with the idea that each and every living thing is related through a common evolutionary heritage. Despite being accepted for about a century and a half, I argue that a truly intuitive grasp of common descent remains difficult. Nevertheless, coming to grips with common descent is of fundamental importance for achieving the central goal of evolutionary biology: to understand the origins of biological diversity. Most notably, I argue that a conspicuously missing topic in evolutionary theory is the explicit comparison of hierarchical patterns and processes of lineage splitting and common descent.

[For brevity, I deleted a part describing Mayr's "horizontal processes" - like speciation; and "vertical processes", like natural selection. These are equivalent to cladogenesis and anagenesis. This horizontal is not to be confused with horizontal gene transfer. I first point out that traits, like teeth vertebrae and eyes, can duplicate within a species by mutation. Therefore, these traits can form phylogenetic trees like gene families. This is the subject of the book, so it's only briefly introduced here.]

1. Common descent is non-intuitive

The most formidable obstacle to a fully intuitive grasp of common descent may be the sheer magnitude of differences that life outwardly expresses. An oak tree and a dung beetle are cousins!? Not to mention our more obscure relatives, the oxymonads, slime molds, and E. coli’s of the world! How can it be that such enormous differences in appearance, life style, size, and behavior have evolved? The answer is not difficult to understand logically. For example, to Darwin the immensity of biotic diversity could in large part be explained by time itself. Geological time is so vast as to be practically incomprehensible. Who then could logically argue with time’s ability to allow for the origin of an equally incomprehensible biological variety – even if starting from a single point? Many of the tell tale similarities expected of cousins would logically erode away after so many millions of generations. But logic quite often does not guide intuition. Such is the case with common descent. Even after learning crystal clear indicators, we continue to be surprised by common descent.

Perhaps the clearest signal of globally shared evolutionary heritage is the genetic code. On October 12, 1962, the headlines of the New York Times read “The Genetic Code is Held Universal: All Living Things Are Said to Use Same Chemicals for Heredity Transfers”[1]. More than a full century after Darwin’s “Origin”, common descent was again in the public eye. Who could help but marvel at the thought of a universal genetic code, in place nearly since the dawn of life? A code that remained constant through the origins of cells, of gastrulation, of brains and of societies. The few exceptions now known to the universal code have not diminished the significance. The conserved hereditary machinery provides a concrete thread linking every organism in the tree of life.

One might expect that the triumphant generality of the genetic code would have precluded any more surprises relating to common descent. After discovering a “universal code”, perhaps we finally could come to grips with the universal relatedness of living things. But more surprises were in store. The advent of molecular developmental genetics would again cause biologists to re-examine their expectations regarding common descent. This time the papers read, “From worms to cows, one class of genes spells out the blueprint”. “Class of genes” of course refers to the Hox genes, the conserved transcription factors involved in body patterning. Discoveries of other genes with highly conserved roles were to follow. Of the gene Pax-6, the newspapers read, “science outdoes fiction” when a human gene was shown to step in seamlessly for a defective fly gene or to produce eyes in unnatural places.

The lesson in this tripartite sketch of the history of biology is that at three levels of organization – species, genes, and developmental processes – biologists have been surprised to discover common descent. To me, this indicates a rather fundamental lack of intuition for the process. We seem to have to relearn the lessons of common descent at every level of biological organization. In each case, we start with the assumption – or perhaps with the notion (something less formal than an assumption) – that biological entities somehow arise de novo in a massively parallel manner. In Darwin’s time very few biologists considered common descent of species (exceptions include Buffon and Erasmus Darwin), and no one else neared the sweeping generalizations for the relatedness of most or all of life that Charles Darwin suggested. Instead, Darwin’s contemporaries and predecessors believed that each species had a separate origin. Some biologists broke the strictly typological thinking common of the time – to Lamark species transformed and to Cuvier they sometimes went extinct – but no one else had formed anything near a Darwinian concept of a global tree of life. Perhaps it is the strong intellectual roots in creationism, or perhaps it is the conceptual difficulty in linking together the entire enormity of biodiversity, but even long after Darwin’s ideas of common descent have been accepted for species, a biologist’s intuition often falls back on the notion of parallel origins when considering other levels of biological organization.

Current support among biologists for common descent of genes (see also this post) is strong– but this was not always so. The 1960’s and early 1970’s was the time when biologists were learning that common descent holds for genes and proteins as well as species. One telling quote, used recently by both Gould {2002} and Carroll {1999}, can be found in an influential book by Ernst Mayr, Animal Species and Evolution.

"Much that has been learned about gene physiology
makes it evident that the search for homologous
genes is quite futile except in very close relatives. If
there is only one efficient solution for a certain
functional demand, very different gene complexes
will come up with the same solution, no matter how
different the pathway by which it is achieved.”

Ernst Mayr (1963)

I do not think that this was a particularly radical viewpoint of the time. For example, I was struck when reading Walter Fitch’s citation classic defining the terms orthology (descent by speciation) and paralogy (descent by duplication), because almost the entire paper is concerned with a topic rather different from orthology vs. paralogy. Instead, Fitch lays out statistical methods for discriminating homologous from analogous proteins. In other words, a real concern of the time was that proteins might have evolved similar sequences in parallel. This is of course a worthy consideration and is a hypothesis that is tested thousands of times per day using similarity searches of genetic databases. Nevertheless, I find comparison with biologists of Darwin’s time extremely interesting. In both cases, massively parallel and de novo evolution was taken almost as the null expectation, no matter how unparsimonious. To Darwin’s contemporaries, species were created separately and similarly. To Fitch’s biochemist and especially to Neo-Darwinist contemporaries of the 1960’s (e.g. Mayr above), the very real possibility remained that genes were “created” separately and similarly in different species. I don’t mean to imply religious-type creationist leanings in the biologists of the 1960’s. On the contrary, their “creator” was strong (Darwinian) natural selection for a particular function. They imagined natural selection to be so powerful and dominant as to allow multiple re-inventions of genes, thereby erasing most of the historical component of genes. No matter the creative force behind the purported independent origins of species or genes, the point here is that deeply rooted common descent was a hard earned realization, not an immediately obvious intuition of biologists studying the problem.

In many ways, it was history repeating in the 1980’s and 1990’s when biologists began discovering deep homologies in body patterning genes like Hox genes. The prevailing view and intuition of the time, especially of morphologists and systematists, was that many organismal structures like segments, eyes, limbs, and hearts, evolved essentially de novo, multiple times independently in various lineages. Like the pre-Darwinian concept of species or the concept of genes in the days preceding the advent of molecular biology, the dogma was that organismal structures and the developmental processes leading to them often arose separately in different lineages – especially when comparing different phyla, which are considered to have different “body plans”. But the discovery of conserved developmental genetic processes for patterning the bodies of taxonomically different organisms forced biologists again to consider common descent at new levels of biological organization.

Eye evolution provides a canonical example. A comprehensive, and well-cited paper on photoreceptors by Salvini-Plawen and Mayr from 1977 surveyed the morphological types of eyes in all animals, concluding that photoreceptors must have evolved essentially de novo 40-65 times independently. But the 1990’s saw a chain of discoveries that showed many genes involved in eye development are homologous between phyla. That visual pigment genes (opsins) are conserved was known for some time. Instead, the watershed discovery in eye evolution was that similar mutant (disease) eye phenotypes in flies, mice and humans are caused by mutations in homologous genes {Quiring, 1994}. These genes are named Pax-6 in vertebrates and eyeless in flies. Multiple other phyla were subsequently shown to utilize homologous Pax-6 proteins during in eye development. Furthermore, multiple other genes besides Pax-6 and opsin were subsequently shown to have a conserved role in eye development across phyla. Similar stories can be told for limbs, hearts, and segments. Naturally, many biologists began to question the generality of the assumption that organs and especially developmental processes evolved multiple times independently. Just as biologists recognized deep common descent of species in the 1860’s and genes in the 1960’s, they began to recognize a real possibility for deep homology at levels of biological organization in between genes and species. These conserved developmental processes and the genes that code for them have been termed “the genetic toolkit for development”.

There are many possible reasons why common descent is hard to intuit, deep-seated intuitions about ladders of progress, and an overemphasis on natural selection seem to be especially important. Yet once we start thinking about genes, traits, and species in terms of common descent, we can be greatly enlightened about how evolution has produced the enormous complexity that we see every day.

---

[1] The Genetic Code is Held Universal. Robert K. Plumb New York Times Octocter 12, 1962.

Pluralistic Darwinism

Every year I ask the undergraduate students in my course EEMB 102-Macroevolution the same question. "What do you think of when I say 'Darwin'"?

Some answers are jokes, like "The Darwin Awards". One common answer, "Darwin's Finches", was unexpected to me. But given the ubiquity of these birds in textbooks, perhaps I should not be surprised. Of course the most common answer is "survival of the fittest".

The reason I ask every year is that I like to point out two things in the first lecture of the course. First, that Darwin was not the only one to think up natural selection. A.R. Wallace famously scooped Darwin, and they published their ideas in 1858 at the urging of Charles Lyell. Two others had actually published the idea of natural selection, long before Darwin and Wallace thought of the idea, but in obscure places. I like to cite this when arguing for science as deterministic - a process unto itself that does not depend much on the individuals who practice it.

The second reason I ask is to highlight that Darwinism is so much more than just natural selection - despite most people's tendency to equate the two. All of the above answers (Darwin Awards, Finches, and survival of the fittest) re-enforce the idea that people often equate Darwinism and natural selection. The Darwin Awards go to people who do stupid things, and thereby "improve the species...by accidentally removing themselves from it". The implicit idea is that removing people with genes coding for stupidity will improve the human species. Much research on Darwin's Finches is about documenting natural selection in the wild. And "survival of the fittest" is the most common buzz phrase referring to natural selection.

Never in my (admittedly small number of) years teaching the course has anyone mentioned any of the other Darwinian Theories (see Mayr's classification), besides natural selection. Why should this be, when global common descent is the most profound idea in all of biology? Global common descent provides explanatory power in biology. It is what scares anti-evolutionists the most, as the realization has transformed the view of humankind's place in the natural world from a self-congratulatory perch atop a Scalae Naturae, to an arbitrary outpost alongside other apes as cousins to every conceivable organism, from slime mold to germ.

It makes me wonder. Why is it that global common descent so often gets such a distant second billing to natural selection? Why do people so often equate Darwinism with natural selection, despite the fact that others conceived of natural selection (unlike global common descent, where as far as I know Darwin was the first) and despite the profound implications of common descent?

One idea is that humans - sometimes even practicing evolutionary biologists - have a difficult time coming to grips with global common descent. Perhaps a branching view of time is difficult to internalize compared to linear time. Perhaps it's all just a vestige of the great chain of being concept.

Questions and realizations about common descent are precisely what I want to contemplate in future posts.