The genome of the relict earless monitor lizard, Lanthanotus borneensis, and the Toxicofera hypothesis

TL;DR

This study sequenced the genome of a rare lizard to better understand the evolution of venom systems and water adaptation in lizards and snakes.

Contribution

The paper provides the first genome assembly of Lanthanotus borneensis and offers new insights into the Toxicofera clade's evolutionary history.

Findings

The Toxicofera clade is supported by multiple gene trees, but relationships within it remain unresolved.

Strong positive selection was found on the titin gene in Toxicofera, especially in snakes.

Low heterozygosity and stable population size suggest resilience but limited adaptive potential in L. borneensis.

Abstract

The earless monitor lizard, Lanthanotus borneensis, is a unique living fossil restricted to the island of Borneo and a possible key to understanding the evolution of the venom delivery system and secondary adaptation to water in lizards and snakes (Squamata).

We sequenced and de novo assembled the genome of L. borneensis to a total size of 1.5 Gbp, 975 contigs with an N50 of 52 Mbp and an L50 of 9. The genome completeness is estimated to be 93% based on the Sauropsida OrthoDB core gene set. A genome-wide set of Lepidosauria orthologs was compiled to reconstruct and date their phylogeny, resulting in 966 protein-coding sequences amounting to a concatenated alignment of 356 kbp with 188 kbp parsimony-informative sites. Based on this phylogenomic analysis, one of the largest of its kind yet conducted for Squamata, we identified that a Toxicofera clade (comprising Serpentes, Anguimorpha, and Iguania) is supported by a plurality of gene trees, but critically, support for relationships within Toxicofera is almost equally distributed amongst the three possible topologies. Our tree-dating confirms a rapid divergence of all major squamate clades within the first 10% of squamate history, which may have contributed to rampant incomplete lineage sorting. While we did not identify positive selection on genes associated with venom components at the base of Toxicofera, our analyses found strong positive selection on the giant protein titin throughout the main clades of Toxicofera and especially in snakes. Genome-wide heterozygosity is low (HO = 0.0004), as is the effective population size towards the present.

Future studies of the evolution of the venom delivery system in Toxicofera require a “true” species tree but also individual gene trees due to incomplete lineage sorting and the concomitant potential for hemiplasy. Titin—a key component of striated muscle elasticity—emerges as a target for future evolutionary studies in Toxicofera and especially in wide-gaped snakes (“Macrostomata”). The low observed genome-wide heterozygosity and the low but stable effective population size of L. borneensis during the large-scale habitat fluctuations on Sundaland in the Quaternary suggest an unexpected resilience to environmental perturbations but also a potentially lowered adaptive potential of this isolated lineage.

The online version contains supplementary material available at 10.1186/s12915-026-02552-4.

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