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. 2015 Dec 4:15:271.
doi: 10.1186/s12862-015-0552-5.

Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants

Bonnie B Blaimer  1 , Seán G Brady  2 , Ted R Schultz  3 , Michael W Lloyd  4 , Brian L Fisher  5 , Philip S Ward  6
Affiliations

Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants

Bonnie B Blaimer et al. BMC Evol Biol. .

Abstract

Background: Ultraconserved elements (UCEs) have been successfully used in phylogenomics for a variety of taxa, but their power in phylogenetic inference has yet to be extensively compared with that of traditional Sanger sequencing data sets. Moreover, UCE data on invertebrates, including insects, are sparse. We compared the phylogenetic informativeness of 959 UCE loci with a multi-locus data set of ten nuclear markers obtained via Sanger sequencing, testing the ability of these two types of data to resolve and date the evolutionary history of the second most species-rich subfamily of ants in the world, the Formicinae.

Results: Phylogenetic analyses show that UCEs are superior in resolving ancient and shallow relationships in formicine ants, demonstrated by increased node support and a more resolved phylogeny. Phylogenetic informativeness metrics indicate a twofold improvement relative to the 10-gene data matrix generated from the identical set of taxa. We were able to significantly improve formicine classification based on our comprehensive UCE phylogeny. Our divergence age estimations, using both UCE and Sanger data, indicate that crown-group Formicinae are older (104-117 Ma) than previously suggested. Biogeographic analyses infer that the diversification of the subfamily has occurred on all continents with no particular hub of cladogenesis.

Conclusions: We found UCEs to be far superior to the multi-locus data set in estimating formicine relationships. The early history of the clade remains uncertain due to ancient rapid divergence events that are unresolvable even with our genomic-scale data, although this might be largely an effect of several problematic taxa subtended by long branches. Our comparison of divergence ages from both Sanger and UCE data demonstrates the effectiveness of UCEs for dating analyses. This comparative study highlights both the promise and limitations of UCEs for insect phylogenomics, and will prove useful to the growing number of evolutionary biologists considering the transition from Sanger to next-generation sequencing approaches.

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Figures

Fig. 1
Fig. 1
Phylogeny of the subfamily Formicinae. Contrasting phylogenetic trees estimated by a the phylogenomic UCE-70 % data set and b the "traditional" Sanger-sequencing-generated 10-nuclear-gene data set. Both figures are based on RAxML best tree searches, with RAxML bootstrap values mapped on the respective nodes. The bootstrap searches included 100 and 1152 replicates for UCE and 10-gene data set, respectively. The six larger formicine tribes are indicated. See also Additional file 8
Fig. 2
Fig. 2
Comparison of support for major lineages within the Formicinae. Comparison of support for formicine tribes and the influence of the problematic taxa. Panel a) UCE-70 % data set, all taxa included; b) 10-gene data set, all taxa included; c) UCE-70 % data set, problematic genera excluded (Santschiella, Gigantiops, Myrmoteras, Oecophylla, Gesomyrmex); d) 10-gene data set, problematic genera excluded. Both figures are based on RAxML bootstrap searches, with 100 and 1152 replicates for UCE and 10-gene data set, respectively. See also Additional file 10
Fig. 3
Fig. 3
a Phylogenetic informativeness and b) comparison of divergence estimates. a Phylogenetic Informativeness (PI) as estimated with TAPIR [41] for the three UCE data sets and the 10-gene data set. PI is here plotted per nucleotide site as it increases with increasing age of divergence (in Ma) between taxa. b Graphic comparison of divergence time estimates for three BEAST analyses (UCE-100best, UCE-95 % and 10-gene data set); node labels correspond with those of Tables 2, Additional file 11, and Fig. 4
Fig. 4
Fig. 4
Time-calibrated phylogeny and ancestral range estimates for the subfamily Formicinae. Maximum clade credibility tree summarized from 48000 trees as estimated with the UCE-100best data set under a relaxed-clock model with nine fossil calibrations. Blue bars show the 95 % highest posterior density range for each node. Node numbers refer to Table 2 and Additional file 11. Ancestral ranges estimated by S-DEC are mapped on MRCA nodes for each tribe and genus (regardless of the level of support) and all other nodes that received high support (>70) for reconstructions. T = Neotropical, N = Nearctic, P = Palearctic, E = Afrotropical, O = Indomalayan and A = Australasian
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