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Research Article
Museomics of tree squirrels: A dense taxon sampling of mitogenomes reveals hidden diversity, phenotypic convergence, and the need of a taxonomic overhaul
Silvia E. Pavan
Museu Paraense Emílio Goeldi; Smithsonian Institution
Corresponding Author
License:
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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.
Keywords
Historical DNA, Morphology, Neotropical region, Phylogeny, Sciuridae
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VLADIMIR DINETS
commented on 20 May, 2020
I wonder why the authors propose splitting a relatively young group into so many small genera instead of simply including Microsciurus into Sciurus.
View 1 reply
Víctor Romero
commented on 11 June, 2020
Congratulations to the authors is an excellent and necessary article. However, I agree with Dinets, I also think it was absolutely necessary to discuss both options
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This is a preprint. It has not completed peer review.
Research Article
Museomics of tree squirrels: A dense taxon sampling of mitogenomes reveals hidden diversity, phenotypic convergence, and the need of a taxonomic overhaul
Silvia E. Pavan
Museu Paraense Emílio Goeldi; Smithsonian Institution
Corresponding Author
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
Prescreen
History
CURRENT STATUS: Posted
Version 1
Posted 14 May, 2020
Community comments: 7
Metrics
Comments: 7
PDF Downloads: ...
HTML Views: ...
License:
This work is licensed under a CC BY 4.0 License. Read Full License
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.
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
VLADIMIR DINETS
commented on 20 May, 2020
I wonder why the authors propose splitting a relatively young group into so many small genera instead of simply including Microsciurus into Sciurus.
View 1 reply
Edson F. Abreu-Jr.
replied on 20 May, 2020
While simpler and perhaps more conservative from a taxonomic perspective, this alternative of grouping all species from Eurasia, Nearctic and Neotropical regions into a single genus (Sciurus) in our opinion would possibly mask important evolutionary and biogeographic information that a more diverse arrangement can provide. Also, this group based on our divergence time estimates (another manuscript under review) is not that young as previous suggested. The entrance of tree squirrels in South America is temporally similar to the arrival of sigmodontine rodents. This last group, although much more diverse in number of species, is split in hundreds of genera. Moreover, just to make clear, we did not described any new genera, we only tentatively applied generic names used in previous taxonomic classifications of Sciurini.
View 1 reply
VLADIMIR DINETS
replied on 20 May, 2020
These are valid arguments, but you also have to consider taxonomic disruption. In any case, I think it's better to discuss both options in the paper.
View 1 reply
Edson F. Abreu-Jr.
replied on 20 May, 2020
Yes, taxonomic disruption indeed has to be taken into consideration. In this case, our taxonomic proposal would have a greater impact on North American taxa, as Central American and South American taxa already are split in four and six genera, respectively (see Vivo and Carmignotto 2015 in Mammals of South America vol. II). Therefore, for Neotropical taxa our arrangement is even less diverse than the current one. One correction from my last comment, sigmodontine rodents are organized in almost a hundred genera in South America (about 90), not hundreds as I mentioned.
View 1 reply
VLADIMIR DINETS
replied on 20 May, 2020
There are also sources that still list almost all Neotropical taxa in Sciurus, such as IUCN and HMW. Anyway, great work, congratulations!
View 1 reply
Edson F. Abreu-Jr.
replied on 20 May, 2020
Thank you!
Víctor Romero
commented on 11 June, 2020
Congratulations to the authors is an excellent and necessary article. However, I agree with Dinets, I also think it was absolutely necessary to discuss both options
Edson F. Abreu-Jr.
replied on 20 May, 2020
While simpler and perhaps more conservative from a taxonomic perspective, this alternative of grouping all species from Eurasia, Nearctic and Neotropical regions into a single genus (Sciurus) in our opinion would possibly mask important evolutionary and biogeographic information that a more diverse arrangement can provide. Also, this group based on our divergence time estimates (another manuscript under review) is not that young as previous suggested. The entrance of tree squirrels in South America is temporally similar to the arrival of sigmodontine rodents. This last group, although much more diverse in number of species, is split in hundreds of genera. Moreover, just to make clear, we did not described any new genera, we only tentatively applied generic names used in previous taxonomic classifications of Sciurini.
View 1 reply
VLADIMIR DINETS
replied on 20 May, 2020
These are valid arguments, but you also have to consider taxonomic disruption. In any case, I think it's better to discuss both options in the paper.
View 1 reply
Edson F. Abreu-Jr.
replied on 20 May, 2020
Yes, taxonomic disruption indeed has to be taken into consideration. In this case, our taxonomic proposal would have a greater impact on North American taxa, as Central American and South American taxa already are split in four and six genera, respectively (see Vivo and Carmignotto 2015 in Mammals of South America vol. II). Therefore, for Neotropical taxa our arrangement is even less diverse than the current one. One correction from my last comment, sigmodontine rodents are organized in almost a hundred genera in South America (about 90), not hundreds as I mentioned.
View 1 reply
VLADIMIR DINETS
replied on 20 May, 2020
There are also sources that still list almost all Neotropical taxa in Sciurus, such as IUCN and HMW. Anyway, great work, congratulations!
View 1 reply
Edson F. Abreu-Jr.
replied on 20 May, 2020
Thank you!