Accumulation of transposable elements inHoxgene clusters during adaptive radiation ofAnolislizards

Abstract

Transposable elements (TEs) are DNA sequences that can insert elsewhere in the genome and modify genome structure and gene regulation. The role of TEs in evolution is contentious. One hypothesis posits that TE activity generates genomic incompatibilities that can cause reproductive isolation between incipient species. This predicts that TEs will accumulate during speciation events. Here, I tested the prediction that extant lineages with a relatively high rate of speciation have a high number of TEs in their genomes. I sequenced and analysed the TE content of a marker genomic region (Hox clusters) in Anolis lizards, a classic case of an adaptive radiation. Unlike other vertebrates, including closely related lizards, Anolis lizards have high numbers of TEs in their Hox clusters, genomic regions that regulate development of the morphological adaptations that characterize habitat specialists in these lizards. Following a burst of TE activity in the lineage leading to extant Anolis, TEs have continued to accumulate during or after speciation events, resulting in a positive relationship between TE density and lineage speciation rate. These results are consistent with the prediction that TE activity contributes to adaptive radiation by promoting speciation. Although there was no evidence that TE density per se is associated with ecological morphology, the activity of TEs in Hox clusters could have been a rich source for phenotypic variation that may have facilitated the rapid parallel morphological adaptation to microhabitats seen in extant Anolis lizards.

Evolutionary lability inHoxcluster structure and gene expression inAnolislizards

“…The mouse, Mus musculus , was chosen as a representative of the most commonly observed tetrapod pattern. The lizards were the two Anolis species with high TE content in Hox clusters ( A. sagrei and A. carolinensis ), one Anolis species ( A. bartschi ) singled out as having unusually low TE content in Hox clusters (Feiner ), and one distantly related lizard (the common wall lizards P. muralis ) with a TE content representative of squamates in general (Fig. ).…”

“…, ; Woltering et al. ; Woltering ; Feiner ). This is hypothesized to be caused by the accumulation of TEs, which are generally excluded from Hox clusters in birds and mammals (Di‐Poï et al.…”

“…I apply a methodology specifically developed to alleviate biases inherent in the annotation of TEs with similarity‐based identifications, and thus offer a comprehensive survey of the TE landscapes of squamate Hox clusters. I also assessed the potential impact of high TE densities within Hox clusters by comparing Hox gene expression patterns during embryonic development in a species with moderate Hox cluster TE density (a Lacertid lizard, the common wall lizard, Podarcis muralis ) and in three species of Anolis lizards, where Hox cluster TE density is highly variable and TE content is particularly high for lineages with high rates of speciation (Feiner ). I therefore compared one Anolis species with low Hox cluster TE density (the West Cuban anole, Anolis bartschi ; Feiner ) with two Anolis species from distantly related clades with high Hox cluster TE densities (the brown anole, A. sagrei and the green anole, A. carolinensis ).…”

The Mobilome of Reptiles: Evolution, Structure, and Function

“…There is no reason to believe that the close examination of reptile genomes would not yield a trove of domesticated TEs. Indeed, the accumulation of TEs in the Hox clusters of reptiles [Di-Poï et al, 2009, which contrast with the extreme structural stability of those clusters in other vertebrates [Deschamps and Duboule, 2017] 29 TE insertions could have had an impact on the morphological diversity of squamates [Di-Poï et al, 2010] as well as the rate of speciation in anoles [Feiner, 2016]. Much work remains to be done to confirm a functional role of those insertions in the evolution of phenotypes.…”

TERAD: Extraction of transposable element composition from RADseq data

“…Ubiquitous among all organisms, TEs are the main contributor of genome size differences across eukaryotes (Gregory, ), and they play a critical role in evolution by introducing mutation and facilitating genomic rearrangement (Bourque et al, ). Cross‐species comparative studies have been instrumental in understanding how ecology affects TE abundance (Kalendar, Tanskanen, Immonen, Nevo, & Schulman, ) and how TEs drive evolution (Feiner, ; Staton & Burke, ).…”