Evolutionary History of the α-Carbonic Anhydrase Gene Family in the Phylum Arthropoda, With Comparisons to αCA in Chordates.

Abstract

The α-carbonic anhydrase (αCA) gene family encodes an abundant and ancient metalloenzyme present in all animals. Found in both eukaryotes and prokaryotes, members of this gene family play vital roles in ionic regulation, acid-base regulation, and respiration. However, little is known regarding the evolutionary history and patterns of molecular evolution of this gene family in the phylum Arthropoda, especially in relation to chordates. Through phylogenetic reconstruction and subcellular localization prediction, we discovered that arthropod αCA genes could be classified into three clades based on phylogenetic topology, as has been found in chordate αCA. Among the three distinct arthropod αCA clades, Clade III, enriched in predicted extracellular and cell membrane-bound subcellular localization, exhibited the highest rates of evolution and greatest number of homologs. Intriguingly, we found distinct patterns of gene family expansions and contractions between arthropods and chordates through gene tree-species tree reconciliation. Lastly, we found that αCA12, a member of Clade III αCA, showed signatures of positive selection (based on dN/dS) in two sibling species within the copepod Eurytemora affinis species complex (E. carolleeae and E. gulfia), compared to the general arthropod αCA background. In these populations, this particular paralog had previously shown contemporary signatures of selection during invasions into novel salinities. Overall, our results indicate that the αCA gene family shows signatures of selection both on macroevolutionary time scales across phyla, as well as between closely related sibling species within Arthropoda.