A bayesian analysis of the genetic evolution in living fossils

Abstract

Most animal species appear radically different from their ancestors that lived hundreds of millions of years ago, yet a few are remarkably similar to their ancient ancestors. Charles Darwin called these ancient-looking creatures living fossils. Genomes of several living fossils, such as the African coelacanth (Latimeria chalumnae) and reptile tuatara (Sphenodon punctatus), were sequenced recently, revealing the low average evolutionary rates of their protein-coding sequences. Such slow genomic and anatomical evolution (i.e., stasis) are poorly understood, especially in the era of big data. For example, how can species evolve slowly despite continual environmental change? Here, we used Bayesian models to (1) quantify how much slower is the genomic (coding sequence) evolution in living fossils than in other species and (2) explain why from a macroevolutionary standpoint. Among vertebrates, we found that, on average, the coding sequence has changed less in living fossil species but only by negligible amounts (-0.02 + or - 0.03 DNA substitutions/site; -0.01 + or - 0.02 amino acids substitutions/site). However, this result is likely due to how researchers classify living fossils. When we focus on the widely recognized living fossils (coelacanth and tuatara), we found that their genomic sequences have evolved less than predicted based on the other species (Bayesian p-values < 0.5). A caveat is that this prediction is sensitive to species sampling. The predictive distributions capture their slow evolution slightly better (increased Bayesian p-values) when the model includes node count, the number of net speciation or branching events along a lineage. The lack of net speciation events in living fossil lineages partly corresponds with their slow genomic evolution, consistent with the theory of punctuated evolution, which posits a coupling between speciation and evolutionary change. Population- and ecological-level processes also dictate rates of evolution, so including them in future models would be crucial. Elucidating speciation as a driver of the pace of living fossils' genomic evolution sheds light on a central problem in evolutionary theory and is essential for conserving these species. An evolutionary history marked by minimal change and a lack of diversity could be costly in today's world of unprecedented climate change.