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Transposable elements unleashed

Mobile DNA sequences – transposable elements or TEs for short – are found in the genome of virtually all organisms. As their name implies, TEs can cut or copy themselves from one location in the genome to another. This can wreak havoc as insertion of TEs may interfere with gene regulation or in fact knock out entire genes. Cells therefore have mechanisms that prevent TEs from jumping, including DNA methylation and other epigenetic tools. Thus, TEs are not roaming freely through the genome, but are restricted from entering functionally important parts. Preventing TE invasion is particularly important when genes are regulated through spatial proximity to each other. The textbook example of this situation are the Hox genes, which are the key players in embryonic development with an ingenious mode of action: Hox genes are arranged in tight clusters and their position in the cluster defines their time and space of expression, and thus their effect on the patterning of the early embryo. It is therefore fitting that Hox gene clusters of mammals and other well-studied vertebrates have been found to be almost completely free of TEs. Nathalie’s new study reveals that Anolis lizards have broken this paradigm. Moreover, the invasion of TEs into Hox clusters of Anolis lizards can be linked to aberrant gene expression and increased rates of speciation.

Ever since the discovery of TEs, people have speculated about their evolutionary implications. One possible consequence of high TE activity is structural genomic variation. This may accelerate genomic incompatibility between populations; effectively making TEs engines of speciation.

Occasionally, TE insertions may also generate phenotypic novelty. As noted above, some genes are regulated through its proximity to other genes, which means that invasion of TEs can change expression of a number of genes simultaneously. Furthermore, since jumping TEs often drag along neighbouring genomic regions, they can translocate regulatory sequences that cause genes to be expressed in new cell types or at different stages in development.

While these are good reasons to expect TEs to promote evolution, examples are few and their role often appears idiosyncratic. An excellent group for a more systematic survey of TE-driven diversification are squamate reptiles, a group that includes lizards and snakes. Squamate genomes do not only appear particularly rich and variable in TEs, but their body plan is also highly malleable. Illustrative examples include the adaptive radiation of Anolis lizards and the repeated evolution of limbless and elongated bodies.

Nathalie decided to study how TEs have shaped the genomes, and in particular, the Hox clusters, of squamates. Her first surprise was to discover that lizards possess more Hox genes than all other tetrapods since they retained some genes that other lineages have ditched. The second surprise came when she looked at the TE content of Hox clusters. Despite the high TE content in their genomes, squamates follow other vertebrates in generally protecting their Hox clusters from TEs. But there was one exception: Nathalie found massive invasion of TEs in the Hox clusters of two out of three Anolis species, with TE contents almost as high as the average place in the genome.

The relationship between TE content in Hox clusters relative to genome-wide TE content in squamate reptiles. All lizards and snakes restrict TEs from their Hox clusters down to roughly half the genome-wide average. However, two Anolis species show Hox clusters that are invaded by TEs, while a third Anolis species (black circle) follows the general trend.

 

Why in Anolis? Anolis lizards are famous in evolutionary biology due to their adaptive morphological radiation involving high rates of speciation – amassing close to 400 species. In a previous study Nathalie showed that Anolis lineages with more speciation events in the past have more TEs in their Hox clusters. This new genome-wide study reveals that this signature of speciation is indeed pronounced in Hox clusters: only the two Anolis species from amply speciating lineages exhibit unusually TE-rich Hox clusters, while a third species (Anolis auratus, black circle in figure above) follows the norm and keeps its Hox clusters relatively free from TEs. Looking in detail at genome-wide TE landscapes of these three Anolis species, Nathalie discovered that the two species with TE-rich Hox clusters had a larger population of young, more active TEs in their genomes. In addition, the inferred timing of peak activity of these TEs broadly coincided with past speciation events.

These results suggest that – during speciation events – TEs are unusually active and proliferate throughout the genome. As a result, even crucial regions such as Hox clusters become invaded. Subsequently, TEs are removed from Hox clusters by selection until a ‘healthy equilibrium’ of TE content relative to the genome-wide TE content is reached. This equilibrium appears highly conserved as the Hox clusters of almost all lizards and snakes contain close to 50% of the global TE content. This proposed model generates a number of predictions that can be tested with genomic data from lineages with variable rates of speciation.

How then do some Anolis species cope with having their Hox clusters invaded by TEs? Clearly, the inflation of Hox clusters – increasing the distance between genes – does not disrupt the patterning of the early embryo. Genes located at one end of the cluster remain expressed early in the head of the embryo, while genes located at the other end are expressed late in the tail. However, the successive activation of Hox genes predicts that disruption, if occurring at all, should be most pronounced towards the end of the Hox clusters. Nathalie found that this indeed is the case: one out of four Hox13 genes showed aberrant expression in the two Anolis species with TE invaded Hox clusters, but this gene was expressed as ‘normal’ in other Anolis and more distantly related lizards.

Expression patterns of the posterior Hox gene HoxD13 are showing variation between species with low and high TE content in their Hox cluster: while expression in limb buds is conserved, expression in tail tissue (black arrows) is missing in species with high TE content in their Hox clusters (A. sagrei and A. carolinensis).

 

Nathalie’s study reveals that, despite being THE textbook example of our conserved developmental toolkit, Hox genes can be tinkered with. What is more, the TE invasion of Hox clusters appear to be intimately linked to diversification. Now that Anolis lizards have shown us that it can happen, perhaps they can also show us why it happens and how.

 

The original version of this blog post was published on the Evolution Letters Editors’ Blog https://evolutionletters.wordpress.com/2019/08/06/the-role-of-mobile-genetic-elements-in-evolution-and-development/

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Hot off the press!

Our book Evolutionary Causation has arrived! It not only looks great, but it also features some really original and exciting ideas by fantastic people. Thanks to all the authors and to the KLI and the MIT Press for making it happen.

Interested in the content? Here is a list of titles and authors:

1 Evolutionary Causation
Tobias Uller and Kevin N. Laland

2 Causality and the Role of Philosophy of Science
Massimo Pigliucci
3 Understanding Bias in the Introduction of Variation as an Evolutionary Cause
Arlin Stoltzfus

4 The Shape of Things to Come: Evo Devo Perspectives on Causes and Consequences in Evolution
Armin P. Moczek

5 Incorporating the Environmentally Sensitive Phenotype into Evolutionary Thinking
David I. Dayan, Melissa A. Graham, John A. Baker, and Susan A. Foster

 6 Genotype-Environment Interaction and the Unscripted Reaction Norm
Sonia E. Sultan

 7 Understanding Niche Construction as an Evolutionary Process
Kevin N. Laland, John Odling-Smee, and Marcus W. Feldman

 8 Biological Dynamics and Evolutionary Causation
Renée A. Duckworth

 9 The Causes of a Major Transition: How Social Insects Traverse Darwinian Space
Heikki Helanterä and Tobias Uller

 10 Are Developmental Plasticity, Niche Construction, and Extended Inheritance Necessary for Evolution by Natural Selection? The Role of Active Phenotypes in the Minimal Criteria for Darwinian Individuality
Richard A. Watson and Christoph Thies

 11 The Paradox of Population Thinking: First-Order Causes and Higher-Order Effects
Denis M. Walsh

 12 Ontology, Causality, and Methodology of Evolutionary Research Programs
Jun Otsuka

 13 A Darwinian Dream: On Time, Levels, and Processes in Evolution
Arnaud Pocheville

 14 Decoupling, Commingling, and the Evolutionary Significance of Experiential Niche Construction
Lynn Chiu

 15 Biological Information in Developmental and Evolutionary Systems
Karola Stotz

 

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Plasticity can take the lead in adaptive evolution

Plasticity-led evolution would be likely if the trait combinations induced by novel environments harbour more than their fair share of genetic variation. Our new paper in PNAS shows that this is in fact quite common. For a nice overview, see this post by Luis-Miguel Chevin on F1000.

Dan Noble and Reinder Radersma collected data from studies that quantified traits and their additive genetic covariance in animals and plants exposed to novel environments. On the whole, the multivariate phenotypic change caused by environmental change were well aligned with the maximum genetic variation – and better than expected by chance.

There are several ways to interpret these results. Perhaps the most interesting from the perspective of evolvability is that developmental systems respond to environmental novelty as they do to genetic mutation. Such developmental bias means that populations that evolve plasticity will tend to continue to evolve in some ways rather than others. The present paper is the first in a series of empirical and theoretical papers that address this problem as part of our group’s involvement in an international research effort. So please keep an eye out for more.

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It is time to say goodbye…

… to Reinder and Alfredo.

As the EES grant comes to a close, we are sad to see some of our friends move on, but excited about the opportunities they have created for themselves.

Reinder is now a researcher in statistical genetics at Wageningen University & Research Institute, which is THE place to be for agriculture, environmental and food science. His work on maternal effects, plasticity and evolvability will undoubtedly prove useful also to domesticated plants and animals.

Alfredo also leaves us, in this case for a postdoc in Copenhagen. After a couple of years with theory, he is now ready to get his hands dirty with data again. The aim is to reveal the molecular complexities of maternal-fetal communication, a perfect opportunity to transfer skills between evolutionary and developmental biology!

Although it is sad for all of us to see them leave, it is particularly sad for Tobias – they have known each other since the Oxford years, when Reinder did a postdoc with Ben Sheldon and Alfredo his MSc with Tobias. They have been fantastic friends and colleagues – always positive, helpful, and engaged. Hats off for everything you have taught us over the years.

See you soon!!

 

 

 

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Summer cottage getaway

All visitors to Sweden should experience that summer cottage feeling! Accordingly, the group packed their thermal underwear, swim trunks, shorts and rain coats and headed to Tobias’ family’s cottage in Värmland. All outfits came to good use since we had typical Swedish summer weather – blue sky followed by rain, and then glorious weather when we had to leave. Just like every year.

View from the veranda on day 1…. and day 2…

Germs, lizards and field work cut our numbers this time. But the rest of us had a great time – relaxing, birding, fishing, swimming, and beaver watching, enjoying local art exhibitions, cultural history, snaps, and grillkvällar… or, to quote Yang: “we managed to do and see everything we were promised – and in addition we watched the Champion’s League final!”

What can we catch here – pike? perch? pikeperch?… hang on, what did you just say!?  
Yang and Roman are off for an adventure! They did come back eventually.

 


A beaver with unfinished business, perhaps the one that swam past this morning?

 


Summer lunch with traditional food, snaps and songs. The students are getting younger every year…

 

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Geoff While visiting

We are very happy to have Geoff While from the University of Tasmania visiting us for three months. Geoff is a fantastic friend and collaborator whose scientific drive, passion for biology, and lizard catching skills are nearly impossible to beat. In addition to the usual wall lizard field season, we have a few old projects to finish off, some that are in full swing, and perhaps one or two new ones to launch. Not to mention all the other things you could get done over a beer or two. Welcome Geoff!

Cheers!

 

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