Museomics of tree squirrels: A dense taxon sampling of mitogenomes reveals hidden diversity, phenotypic convergence, and the need of a taxonomic overhaul

Abstract

Background: Tree squirrels (Sciuridae, Sciurini), in particular the highly diverse Neotropical lineages, are amongst the most rapidly diversifying branches of the mammal tree of life but also some of the least known. Negligence of this group by systematists is likely a product of the difficulties in assessing morphological informative traits and of the scarcity or unavailability of fresh tissue samples for DNA sequencing. The highly discrepant taxonomic arrangements are a consequence of the lack of phylogenies and the exclusive phenotypic-based classifications, which can be misleading in a group with conservative morphology. Here we used high-throughput sequencing and an unprecedented sampling of museum specimens to provide the first comprehensive phylogeny of tree squirrels, with a special emphasis on Neotropical taxa. Results: We obtained complete or partial mitochondrial genomes from 232 historical and modern samples, representing 40 of the 43 currently recognized species of Sciurini. Our phylogenetic analyses - performed with datasets differing on levels of missing data and taxa under distinct analytical methods - strongly support the monophyly of Sciurini and consistently recovered 12 major clades within the tribe. We found evidence that the diversity of Neotropical tree squirrels is underestimated, with at least six lineages that represent taxa to be named or revalidated. Ancestral state reconstructions of number of upper premolars and number of mammae indicated that alternative conditions of both characters must have evolved multiple times throughout the evolutionary history of tree squirrels. Conclusions: Complete mitogenomes were obtained from museum specimens as old as 120 years, reinforcing the potential of historical samples for phylogenetic inferences of elusive lineages of the tree of life. None of the taxonomic arrangements ever proposed for tree squirrels fully corresponded to our phylogenetic reconstruction, with only a few of the currently recognized genera recovered as monophyletic. By investigating the evolution of two morphological traits widely employed in the taxonomy of the group, we revealed that their homoplastic nature can help explain the incongruence between phylogenetic results and the classification schemes presented so far. Based on our phylogenetic results we suggest a tentative supraspecific taxonomic arrangement for Sciurini, employing 13 generic names used in previous taxonomic classifications.