Saturday, May 31, 2008

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.


chuckgoecke said...

"cousins to every palm, gastrotrich, and canary" Nice. Permission to steal? Naw, I wouldn't. Nice blog!

Hunter said...

Now I know where to go when I want some heavy-duty evolutionary theory. Thanks!

Maybe it's just my eclectic (and sometimes pretty random) education, or maybe it's just being a Pagan, but I have no problems with common ancestry at all. Makes perfect sense to me.

Kosmo said...

Nice to see a new fellow blogger. Great space you've got here. Keep it up.

caiuscamargarus said...

For some unsolicited advice: people might get the "palm, gastrotich and canary" more if it scans a little closer to the original Tom, Dick and Harry. Might I suggest changing "gastrotich" to just plain "tick"?

Great post though!