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

Citation

Abreu-Jr, Edson F. et al. (2020), Museomics of tree squirrels: a dense taxon sampling of mitogenomes reveals hidden diversity, phenotypic convergence, and the need of a taxonomic overhaul, Dryad, Dataset, https://doi.org/10.5061/dryad.9w0vt4bc9

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 phylogeneticists is likely a product of the scarcity or unavailability of fresh tissue samples for DNA sequencing. Lack of comprehensive phylogenies result in highly discrepant taxonomic arrangements that are based exclusively on morphological data—impressively, these are the only classification schemes available for the group. Here we used high-throughput sequencing and an unprecedented sampling effort of museum specimens to provide the first comprehensive phylogenetic analysis of tree squirrels, with a special emphasis on Neotropical taxa. Results: We gathered mitochondrial genome data from 232 modern and historical samples, representing 40 out of the 43 currently recognized species of Sciurini. We found no correlation between specimen age and completeness of mitogenomes recovered for historical samples. Our phylogenetic analyses—performed with datasets differing on levels of missing data and taxa under distinctanalytical 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 seven lineages that might represent taxa to be named or revalidated. Ancestral state reconstructions of number of upper premolars and number of pairs of mammae indicated that alternative conditions of both characters must have evolved multiple times along the evolutionary history of tree squirrels. Conclusions: We were able to obtain complete mitogenomes for samples as old as 120 years, reinforcing the potential of historical samples for phylogenetic and evolutionary 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 to explain the incongruence between phylogenetic results and classification schemes presented so far, and we recommend a substantial taxonomic overhaul.

Usage Notes

Datasets used on the phylogenetic analyses of the tribe Sciurini, generated considering distinct percentages of mitogenome completeness per sample, as follow: Dataset 1 included only complete mitochondrial genomes (92 specimens with no missing data); Dataset 2 included samples with at least 80% of the mitogenome (162 specimens with <20% of missing data per sample); Dataset 3 included samples with at least 60% of the mitogenome (186 specimens with <40% of missing data per sample); Dataset 4 included samples with at least 40% of the mitogenome (210 specimens with <60% of missing data per sample); and Dataset 5 included samples with at least 20% of the mitogenome (232 specimens with <80% of missing data per sample).

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico, Award: 147145/2016-3,203692/2017-9,165553/2017-0,304156/2019-1

American Society of Mammalogists, Award: Latin American Student Field Research Award

American Museum of Natural History, Award: Collection Study Grant

Smithsonian Institution, Award: Postdoctoral Fellowship,Postdoctoral Fellowship

National Geographic Society, Award: NGS-381R-18,Support for Women + Dependent Care – 3758

Fundação de Amparo à Pesquisa do Estado de São Paulo, Award: 09/16009-1