University of Bristol team shows squamates expanded up to 74 million years earlier than thought

Dating the expansion of a group of species when the fossil record is sparse is not a simple task, and can change as methods of analysis become more sophisticated.

Squamates, for example, a grouping that includes lizards, snakes and their relatives, is thought to have expanded about 100 million years ago, coinciding with the Cretaceous Terrestrial Revolution when there was a surge of species growth. Recently, however, a group of scientists from the University of Bristol in the United Kingdom has argued that the squamate diversity explosion occurred much earlier, about 174 million to 145 million years ago in the Middle to Late Jurassic period.

Their research appears in the journal eLife, May 3.

The researchers acknowledge a Cretaceous expansion of squamates is plausible because of the explosion of diverse insect populations at that time. However, they provide evidence of their new dating showing that the squamates arose and "established their key ecological roles much earlier than had been assumed, and have not changed them much since."

Lead author Arnau Bolet, a postdoctoral researcher at Institut Català de Paleontologia Miquel Crusafont and senior research fellow at the University of Bristol School of Earth Sciences, summarized their thesis in an interview.

"Basically, our analyses show that squamates, according to the morphology of the known fossils, laid the groundwork of their evolutionary success in the Jurassic," Bolet said. "The idea that squamates might have diversified in the Jurassic is not new but it arose from a direct and qualitative interpretation of the fossil record, and we have been able to validate it through the use of numerical quantitative methods."

"The original idea was that the evolutionary relationships of squamates, combined with the ages of the few recorded Jurassic forms, suggested that a good part of their evolutionary history had to have occurred in the Jurassic," he added. "Our study provides support to this thesis by analyzing the information stored in morphological datasets."  

Lepidosaur morphospace

The researchers start with evidence concerning lepidosaurs—a Greek word for scaled reptiles—the family that includes squamates. As they emphasize, these squamates "are one of the most species-rich tetrapod clades [groups with a common ancestor], only rivaled by birds in terms of diversity among tetrapods." But unlike birds, the record is uncertain about when the squamates acquired "their current range of ecological adaptations."

To make their case, the scientists look at morphospace distribution and phylogenetic comparative methods.

"Morphospaces are maps showing how shapes are defined by quantitative or qualitative traits," Bolet said.  "In our study we used morphological discrete characters for an exhaustive list of fossil and extant lepidosaurs--mostly squamates--to build a morphospace that is then summarized in 2D or 3D plots. Such plots illustrate the similarity or dissimilarity between forms by placing species that are more similar in a closer position.

"By looking at how morphospace distribution changes through time, together with other measures, we can make inferences on the timing of key events in the evolutionary history of a group," Bolet added.

Phylogenetics and a numerical approach

The other type of evidence the researchers used is phylogenetics, the study of  the evolutionary history of a group, which can be inferred from the heritable traits and morphology.

Bolet said "a phylogenetic tree is a graphical representation in the form of a branching diagram, or tree, of the hypothetical evolutionary relationships of a number of biological species, based upon similarities and differences in their morphological or genetic characteristics. In the case of our study, the same morphological characters were used to calculate the morphospace and the phylogenetic tree."

"Our analyses of phylogenetic relationships, morphospace distribution and evolutionary rates correspond to a numerical approach that provides support to the idea of a Jurassic radiation of squamates in a quantitative way and represent a step forward in the analysis of the origins of squamate diversity," Bolet added.

Figure 1 in the article depicts the lepidosaur morphospace through time. 

“Stepping up through time, from bottom to top of the stack, shows how lepidosaur morphospace expanded, not gradually, but marked by a single major step,” in the Middle-Late Jurassic," the article noted. "Our interpretation of the long-term stable morphospace occupation by squamates is compelling because the apparent increase in species richness through time, even if partially influenced by bias in the fossil record, is not linked to a great increase in occupied morphospace."

The article also notes, "the great expansion in [squamate] species numbers up to 10,000 today and has happened partly by minor expansions of the total morphospace envelope, but mainly by packing ever more species inside the existing morphospace area."

Asked if this non-gradual increase surprised the researchers, Bolet said, "What surprised us was to recover such a strong signal supporting the Jurassic rise of squamates, given the small number of available fossils of the group of this particular age."

"In some occasions an enhanced fossil record, like the one occurring in the Late Cretaceous can overprint this signal and make other periods --mainly those with a much poorer record, like the Jurassic in the case of squamates--look less important in the evolutionary history of a group, almost as if nothing important was happening then," he said. "We think that if more Jurassic squamates are discovered, these will provide additional support for our thesis."

Next steps  

Bolet concluded "squamates, despite representing a great portion of extant tetrapods--they are more diverse than mammals, and almost as diverse as birds--do not always get the attention they deserve."

The researchers' next steps, he said, "will be to refine our methods in order to recover more robust results, mainly regarding how we calculate the age one species diverged from its closest relative, one of the main aspects that can influence other results like those of evolutionary rates."

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A. Bolet et al. The Jurassic rise of squamates as supported by lepidosaur disparity and evolutionary rates, eLife, May 3, 2022

DOI:  https://doi.org/10.7554/eLife.66511