Interrogating Genomic-Scale Data to Resolve Recalcitrant Nodes in the Spider Tree of Life

Abstract

Genome-scale data sets are converging on robust, stable phylogenetic hypotheses for many lineages; however, some nodes have shown disagreement across classes of data. We use spiders (Araneae) as a system to identify the causes of incongruence in phylogenetic signal between three classes of data: exons (as in phylotranscriptomics), noncoding regions (included in ultraconserved elements [UCE] analyses), and a combination of both (as in UCE analyses). Gene orthologs, coded as amino acids and nucleotides (with and without third codon positions), were generated by querying published transcriptomes for UCEs, recovering 1,931 UCE loci (codingUCEs). We expected that congeners represented in the codingUCE and UCEs data would form clades in the presence of phylogenetic signal. Noncoding regions derived from UCE sequences were recovered to test the stability of relationships. Phylogenetic relationships resulting from all analyses were largely congruent. All nucleotide data sets from transcriptomes, UCEs, or a combination of both recovered similar topologies in contrast with results from transcriptomes analyzed as amino acids. Most relationships inferred from low-occupancy data sets, containing several hundreds of loci, were congruent across Araneae, as opposed to high occupancy data matrices with fewer loci, which showed more variation. Furthermore, we found that low-occupancy data sets analyzed as nucleotides (as is typical of UCE data sets) can result in more congruent relationships than high occupancy data sets analyzed as amino acids (as in phylotranscriptomics). Thus, omitting data, through amino acid translation or via retention of only high occupancy loci, may have a deleterious effect in phylogenetic reconstruction.

Keywords: Araneae; noncoding regions; phylogeny; target-capture; transcriptomics.

Fig. 1.

Maximum likelihood phylogeny of spiders resulting from the AllUCEs10 data set (occupancy 10, 1,060 loci) collapsed to family level. Paraphyly is indicated by vertical violet bars. (A) All major lineages of spiders at family level except the RTA Clade and Araneoidea; (B) RTA Clade; (C) All 17 families of superfamily Araneoidea. The rhombi at the nodes indicate four support values: Shimodaira–Hasegawa-like approximate likelihood ratio test (left top), ultrafast bootstrap (right top), gene concordance factor (gCF) (left bottom), and site concordance factor (sCF) (right bottom). The numbers at the node indicate clades as described. Branch lengths are not to be scaled. For the original sampled tree, see supplementary figure 2, Supplementary Material online.

Fig. 2.

Maximum likelihood phylogenies of spiders resulting from different data sets at various occupancies. Each colored box indicates a data set corresponding to supplementary table 2, Supplementary Material online. The first and second rows represent phylogenies resulting from data analyzed as nucleotides and amino acids, respectively, of codingUCEs (outlined red) and AllUCEs (outlined blue).

Fig. 3.

Comparison of phylogenetic relationships between (A) transcriptomic phylogeny as published by Fernández et al. (2018) using amino acids, and (B) nucT (Fernández et al. 2018, transcriptome data set analyzed as nucleotides). Both phylogenies were constructed using occupancy of 67%. The highlighted blue box indicates Araneoidea families.

Fig. 4.

Comparison of interfamilial relationships of Araneoidea. (A) AllAAUCEs tree, (B) AllUCEs tree. Occupancy of both phylogenies was 10%. Colored branches indicate family relationships that are congruent in both trees.

Fig. 5.

Schematic representation of data classes analyzed in this study in a maximum likelihood framework. Squares indicate original data sets from Fernández et al. (2018) and Kulkarni et al. (2020), and circles indicate matrices analyzed in our study. Circles with red outline indicate amino acid data set, black outline indicates noncoding region data set, and the circles with outline indicate nucleotide data sets. UCE, ultraconserved elements.