Green Anoles, Genomic Evolution And Surfing (Wait, What?)

She’s looking at me, probably thinking “Will he eat me”? And I’m looking at her, thinking “How many transposable elements are in your genome?”

I wanted to bring the attention of the Anolis community to our recent publication in Genome Biology and Evolution (Tollis and Boissinot 2013), where we study the population dynamics of those fascinating features of the green anole genome – transposable elements. Transposable elements (TEs) are important components of vertebrate genomes that may seem a bit esoteric to many readers of this blog, yet the Anolis genome has already yielded great insights into how the vertebrate classes differ in terms of these DNA parasites. In a nutshell, our paper shows how microevolutionary forces such as natural selection and genetic drift account for differences which are most obvious when we make macroevolutionary comparisons (i.e. between mammals and reptiles). Even though I’ve cut to the chase a little early, I thought it might be nice to discuss what we know about the study of genomic evolution, and how the Anolis genome is contributing to the field of comparative genomics.

For a group occupying such a small branch on the tree of life (they aren’t even visible on this eukaroytic evolutionary tree), vertebrates show a lot of variation in their genome sizes. One can visit the Animal Genome Size Database (www.genomesize.com) and see that there are currently 3226 vertebrates for which there are genome size estimates, the smallest being the green pufferfish Tetraodon fluviatillis at 0.35 pg, and the largest being the marbled lungfish Protopterus aethiopicus at 132.83 pg (a picogram, or pg, is roughly equivalent to the mass of 1Gb of DNA). This is an incredible range, and where does A. carolinensis fit in? Its genome is estimated to be 2.2Gb in size, which is actually right around the average for lizards (~2.12Gb) and snakes (~2.08Gb).

(**Note** for some reason, the database treats lizards and snakes as separate groups, which we know here to be a false dichotomy since snakes are phylogenetically nested within lizards, but we can leave it be since their average genome sizes are about the same.)

Vertebrates also vary in terms of their genome structure. For instance, Fujita et al. (2011) showed how the Anolis genome is remarkably uniform in its GC content, unlike the human and chicken genomes, which have isochores. This realization led to the suggestion that GC content may not be as integral to genomic stability as once thought. Way to go, green anole, for bucking the trend!

What drives the evolution of genome size and structure? Some have argued that natural selection plays a large role. For instance, every time powered flight has evolved in a vertebrate lineage (three times, of course – first in pterosaurs, then dinosaurs, then bats) it was accompanied by a sharp reduction in genome size (Organ and Shedlock 2009). This suggests that shedding DNA may have some kind of adaptive value related to flight.

There is another explanation for the observed variation in genomic complexity. In a very important paper, Lynch and Conery (2003) demonstrated that the switch between the small and simple genomes of prokaryotes and the large and complex genomes of eukaryotes is highly correlated with a sharp reduction in effective population size (Ne). From the basic principle of population genetics which states that purifying selection cannot remove deleterious alleles as efficiently in small populations, Lynch and Conery suggest that the accumulation of “junk DNA” such as TEs may have more to do with genetic drift.

So, which is controlling genome size and structure – selection or drift ? This is the main question of comparative genomics, and it is unresolved. Enter A. carolinensis. We thought the little green fellas could help shed light on this conundrum, due to the complete genome sequence, a recent evolutionary history that has been well studied, and relatively easy access to natural populations. Since TEs are responsible for so much of the variation in genome size and structure between vertebrates, we looked in each of five green anole populations and measured the allele frequencies of long and short copies of L1 retrotransposons, which are a type of TE that dominates the human genome (Lander et al. 2001). We have two main conclusions:

1) Purifying selection controls TEs in Anolis: Full-length (FL) L1 retrotransposon copies are less frequent in green anole populations than truncated (TR) ones. This suggests that long elements are deleterious alleles which can cause harmful mutations such as ectopic recombination (Langley et al. 1998), as shown in Drosophila (Petrov et al. 2003), human (Boissinot et al. 2006) and stickleback fish (Gasterosteus aculeatus) (Blass et al. 2012).

2) The strength of selection against TEs is highly dependent on host demography history. This is the exciting thing we learned in our analysis. Although FL L1s are rare in all populations, they are found at significantly higher frequencies in the two U.S. mainland populations: North Carolina, which has the smallest estimated Ne of the five described populations (Tollis et al. 2012) and the Gulf-Atlantic, which likely experienced a recent westward range expansion (Campbell-Staton et al. 2012, Tollis et al. 2012). Both of these populations are candidates for situations where genetic drift is very strong. Meanwhile, the Florida green anole populations, which are older and putatively more demographically stable (Campbell-Staton et al. 2012, Tollis et al. 2012), maintain their FL L1s at significantly lower frequencies. This suggests that in populations of large Ne, deleterious alleles are more successfully held at bay by stronger purifying selection.

Demographic context of green anole populations across the species’ natural range (summarized from Tollis et al. 2012 and Campbell-Staton et al. 2012). The continental mainland populations (North Carolina and Gulf-Atlantic) are likely subjected to stronger genetic drift.

Our work with A. carolinensis shows that while purifying selection has some ability to control the fate of TEs in reptile genomes, the demographic histories of populations can drive the evolution of many important features. The waxing and waning of Ne that may occur during the lineage diversification process may have profound effects on the genomic differences we observe at wider taxonomic scales.

What about the surfing? Alleles at the expansion wave front

Silly me, I almost forgot. One discovery that is buried in our new paper is related to the effects of demographic range expansions on genetic variation. It has been shown that the wave front of an expansion creates a situation where pockets of demes are subjected to very strong genetic drift due to repeated founder events , causing otherwise deleterious alleles to become fixed in populations (Peischl et al. 2013 does a great job of describing this, and it was just made available as our paper went into press). This was perhaps most notably described in European human populations (Lohmueller et al. 2008), but also more recently shown in Old World tortoises (Gracia et al. 2013). We show a second example of reptilian allele “surfing” in the Gulf-Atlantic green anole population, which recently expanded across the Gulf-Coastal Plain, across the Mississippi River and into Texas. Deleterious FL L1 retrotransposon insertions are much more likely to be fixed in this population (in fact, there are no fixed FL L1 in Florida). So, as the lizards moved west, their intragenomic parasites caught the wave and… “YEEEE-HAW” (or maybe I should say “Cowabunga”, or something).

I can’t believe I wrote “cowabunga” in a blog post…

Tollis, M and Boissinot, S. (2013). Lizards and LINEs: Selection and Demography Affect the Fate of L1  Retrotransposons in the Genome of the Green Anole (Anolis carolinensis). Genome Biology and Evolution. 5 (9):1754-1768. doi: 10.1093/gbe/evt133.

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Marc Tollis

Postdoc, Arizona State University.

I study comparative genomics of reptiles, birds, and mammals to understand substitution rate variation across lineages, the link between genotypes and phenotypes, and the evolution of cancer suppression.

Latest posts by Marc Tollis (see all)

• Hundreds of Genes Help to Resolve Green Anole Evolutionary History in North America - October 24, 2016
• The Genetics of Anolis Lizard Tail Regeneration: (Re)generating Major Internet Buzz - August 29, 2014
• Green Anoles, Genomic Evolution And Surfing (Wait, What?) - October 3, 2013