Whole Genomes Reveal Evolutionary Relationships and Mechanisms Underlying Gene-Tree Discordance in Neodiprion Sawflies

• Published in: Systematic biology 2024-10, Vol.73 (5), p.839-860
• Main Authors: Herrig, Danielle K, Ridenbaugh, Ryan D, Vertacnik, Kim L, Everson, Kathryn M, Sim, Sheina B, Geib, Scott M, Weisrock, David W, Linnen, Catherine R
• Format: Article
• Language: English
• ISSN: 1063-5157; 1076-836X; 1076-836X
• DOI: 10.1093/sysbio/syae036

Abstract Rapidly evolving taxa are excellent models for understanding the mechanisms that give rise to biodiversity. However, developing an accurate historical framework for comparative analysis of such lineages remains a challenge due to ubiquitous incomplete lineage sorting (ILS) and introgression. Here, we use a whole-genome alignment, multiple locus-sampling strategies, and summary-tree and single nucleotide polymorphism-based species-tree methods to infer a species tree for eastern North American Neodiprion species, a clade of pine-feeding sawflies (Order: Hymenopteran; Family: Diprionidae). We recovered a well-supported species tree that—except for three uncertain relationships—was robust to different strategies for analyzing whole-genome data. Nevertheless, underlying gene-tree discordance was high. To understand this genealogical variation, we used multiple linear regression to model site concordance factors estimated in 50-kb windows as a function of several genomic predictor variables. We found that site concordance factors tended to be higher in regions of the genome with more parsimony-informative sites, fewer singletons, less missing data, lower GC content, more genes, lower recombination rates, and lower D-statistics (less introgression). Together, these results suggest that ILS, introgression, and genotyping error all shape the genomic landscape of gene-tree discordance in Neodiprion. More generally, our findings demonstrate how combining phylogenomic analysis with knowledge of local genomic features can reveal mechanisms that produce topological heterogeneity across genomes.