Which came first, the bird or the smaller genome?

by Stephen F. Matheson
Originally published on Quintessence of Dust, August 2007.

It’s easy to think of a genome as a collection of genes, perhaps because so many of the metaphors
used to explain genes and genomes (blueprint, book of life, Rosetta Stone) can give one the
impression that everything in a genome is useful or functional. But genomes are, in fact, packed
with debris. Many genomes contain huge collections of fossil genes: genes that have been
inactivated by mutation but were never discarded, sort of like the old cheap nonfunctional VCRs in
my basement. And many genomes contain even more massive collections of another kind of fossil-
like DNA: mobile elements, or their remnants. The human genome, for example, contains over 1
million copies of a single type of mobile genetic element, the Alu transposon. Together, the various
types of mobile genetic elements comprise nearly half of the human genome.

Think about that. Almost half of the human genome is made up of known mobile elements, pieces
of DNA that can move around, either within a genome or between genomes with the help of a virus.
This extraordinary fact – and many of the specifics surrounding it – constitutes one of the most
compelling sources of evidence in favor of common descent, the kind of data for which only
common ancestry provides a complete (or even reasonable) explanation. I’ll come back to this topic
regularly.

Now it turns out, not surprisingly, that differences in genome size among types of organisms are
determined primarily by the numbers of these mobile elements, and not by the number of genes. In
fact, there is wild variation in genome size among types of organisms, and the variation has little to
do with the numbers of genes expressed by those organisms. Consider birds, the subject of a 2007
report in Nature (“Origin of avian genome size and structure in non-avian dinosaurs,” Organ et al.,
8 March 2007).

Birds have remarkably small genomes, averaging 1/2 to 1/3 of the size of typical mammalian
genomes. (The chicken genome, for example, is less than half the size of the mouse genome.) Why
might this be? In other words, how might we explain this difference? The authors point to two
important ideas. First, the chicken genome has been fully sequenced and analyzed, and it contains
far less of the debris mentioned above. It seems that the processes that create (or multiply) mobile
genetic elements are significantly less active in birds than in mammals and other vertebrates.
Second, small genome size is intriguingly correlated with flight. Bats, compared to other mammals,
have small genomes, and flightless birds, compared to other birds, have larger genomes. This has
led to the proposal that small genome size might offer a selective advantage to flying animals, by
reducing the energy cost associated with hauling all that debris around. So, it seems that a smaller
genome is advantageous for flying vertebrates, and that genome size can be reduced by restraining
the production of mobile genetic elements. And this raises several interesting questions, including
this one: did the reduction in genome size accompany the origin of bird flight, or did it happen in
advance? In other words, we can propose at least two alternative scenarios:

1) flight drove the genome change, by favoring small genomes, or

2) the genome change happened first, and helped to get flight off the ground.

How can we even hope to distinguish between these possible explanations? We would need,
somehow, to look at the genomes of the ancestors of birds. And all evidence indicates that the
relevant ancestors of birds are dinosaurs; in fact, today's birds are considered to be flying

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dinosaurs. The recent description of protein sequences from T. rex bone provided strong
confirmation of the birds-from-dinosaurs hypothesis, but no DNA was recovered from the samples,
and no information about genome structure can be inferred from those otherwise fascinating
studies. If only, a la Jurassic Park, we could get some dino DNA...

Enter Organ et al. with a wonderfully creative idea. It turns out that, in organisms alive today, cell
size is strongly correlated with genome size. In other words, organisms with large genomes tend to
have larger cells. This relationship was first described in red blood cells, but Organ et al. show that
it holds quite well in bone cells as well. Using bones from living species, they created a statistical
model that enabled them to infer genome size by looking at the size of bone cells. Then they
combined their model with measurements of bone cell size from fossilized bones of long-extinct
animals, and were able to estimate the genome size of dozens of extinct species, including 31
dinosaur species and several extinct bird species. Their results are remarkable: small genomes are
found in the entire lineage (with one interesting exception, Oviraptor) that gave rise to birds, all
the way back to the theropod dinosaurs that are the typical reference point in the dinosaur-to-bird
story. Here's how the authors put it: "Except for Oviraptor, all of the inferred genome sizes for
extinct theropods fall within the narrow range of genome sizes for living birds." Even if you don't
have access to Nature, you can have a look at the cool family tree in Figure 2, which shows small
genomes in red and larger ones in blue. It's a compelling image.

The results suggest that small genomes arose long before dinosaurs took to the air, and raise some
interesting questions about the interplay of physiological function (e.g., energy consumption
associated with flight) and genome structure. Certainly scenario #1 above is not favored by these
findings: flight apparently arose in organisms that already had much smaller genomes than many
of their earthbound cousins. The relationship between flight and small genome size, then, remains
unclear and even mildly controversial. Organ et al. acknowledge that the two characteristics did not
arise together, but after reference to the larger genomes in flightless birds, they conclude their
paper by noting that "the two may be functionally related, perhaps at a physiological level." And
they postulate that small genome sizes may have been favored by warm-bloodedness and its
associated energetic demands. But a minireview of the paper raises several criticisms of these
hypotheses, and it is clear that the evolutionary forces acting on genome size are complex and yet
poorly understood.

Notwithstanding the unanswered questions regarding genome evolution, this paper is the kind of
scientific article that should be carefully considered by those who deny common descent. Following
are some aspects of the story that create interesting questions for creationists and/or design
advocates.

Consider the results presented in Figure 2. Outside of common ancestry, how are we to account for
these data? The strong correlation between flight and small genome size in living organisms might
look like some kind of "design" to someone who favors that sort of thinking, but Organ et al. have
conclusively uncoupled genome size and flight. Of course those of us who see the universe as a
creation will be happy to marvel at the advantages presented by small genomes to flying organisms,
and perhaps we'll all think of these wonders as evidence of brilliant "design." But it seems to me
that "design" does not serve a significant explanatory role here. On the contrary, I maintain that
the work of Organ et al. demonstrates the following: in dinosaur lineages, the best way to predict
genome size in an extinct species is to know the ancestry of the species. Common design aspects

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don't help. Common descent explains the pattern.

And yet, I think it gets much worse than that for anti-evolution thinkers. I regularly see certain old-
earth creationists (e.g. the folks at Reasons To Believe) and design proponents (e.g. William
Dembski) arguing that "junk DNA" (which includes, but is not limited to, the 45% of the human
genome composed of mobile elements and their debris) is not "junk" but can have important
functions. (The arguments of these critics are flawed in several ways, which I'll detail some other
time.) While it's true that mobile elements have contributed to the formation of new genes from
time to time, and are thought to be significant sculptors of genomic evolution, it's also true that
mobile elements are indiscriminate in their jumping, and their continued hopping about is a
documented cause of harmful mutation. Here, though, is a significant quandary for a design
advocate considering a bird genome: if these mobile elements have important functions in the
organism, then how is it that birds can get by with 1/4 as many of them as, say, squirrels? Why, if
these elements have important functions in the organism, do bats seem to need far fewer of them
than, say, rats? (The genome of the big brown bat is 40% the size of the genome of the aardvark.
Hello!) It seems to me that these facts are best understood when one considers the possibility that
most of this DNA is essentially parasitic, and that some types of organisms have benefited by
restraining its spread. A "design" perspective with regard to genome size is just not helpful, and if
that perspective insists on excluding common ancestry, then it's worse than worthless.

Article(s) discussed in this post:

Organ, C.L., Shedlock, A.M., Meade, A., Pagel, M. and Edwards, S.V. (2007) Origin of
avian genome size and structure in non-avian dinosaurs. Nature 446:180-184.