skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Evaluating UCE Data Adequacy and Integrating Uncertainty in a Comprehensive Phylogeny of Ants
Abstract While some relationships in phylogenomic studies have remained stable since the Sanger sequencing era, many challenging nodes remain, even with genome-scale data. Incongruence or lack of resolution in the phylogenomic era is frequently attributed to inadequate data modeling and analytical issues that lead to systematic biases. However, few studies investigate the potential for random error or establish expectations for the level of resolution achievable with a given empirical data set and integrate uncertainties across methods when faced with conflicting results. Ants are the most species-rich lineage of social insects and one of the most ecologically important terrestrial animals. Consequently, ants have garnered significant research attention, including their systematics. Despite this, there has been no comprehensive genus-level phylogeny of the ants inferred using genomic data that thoroughly evaluates both signal strength and incongruence. In this study, we provide insight into and quantify uncertainty across the ant tree of life by utilizing the most taxonomically comprehensive ultraconserved elements data set of ants to date, including 277 (81%) of recognized ant genera from all 16 extant subfamilies, and representing over 98% of described species. We use simulations to establish expectations for resolution, identify branches with less-than-expected concordance, and dissect the effects of data and model selection on recalcitrant nodes. Simulations show that hundreds of loci are needed to resolve recalcitrant nodes on our genus-level ant phylogeny. This demonstrates the continued role of random error in phylogenomic studies. Our analyses provide a comprehensive picture of support and incongruence across the ant phylogeny, while offering a more nuanced depiction of uncertainty and significantly expanding generic sampling. We use a consensus approach to integrate uncertainty across different analyses and find that assumptions about root age exert substantial influence on divergence dating. Our results suggest that advancing the understanding of ant phylogeny will require not only more data but also more refined phylogenetic models. We also provide a workflow for identifying under-supported nodes in concatenation analyses, outline a pragmatic way to reconcile conflicting results in phylogenomics, and introduce a user-friendly locus selection tool for divergence dating.  more » « less
Award ID(s):
2026772
PAR ID:
10643664
Author(s) / Creator(s):
; ; ; ; ; ;
Editor(s):
Faircloth, Brant
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Systematic Biology
ISSN:
1063-5157
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Blaimer, Bonnie (Ed.)
    Abstract A rapid proliferation in the availability of whole genome sequences (WGS), often with relatively low read depth, offers an unprecedented opportunity for phylogenomic advances using publicly available data, but there are several key challenges in applying these data. Using low‐coverage WGS data for the ant species ofFormica, we conducted detailed comparisons on two different analytical pipelines (reference‐based vs. de novo genome assembly), four types of datasets (5‐kbp‐window, ultra‐conserved element [UCE], single‐copy ortholog [BUSCO] and mitogenome), and a series of analytical procedures (e.g. concatenation vs. coalescent analyses) to identify which are robust to typical WGS data. The results show that at a shallow scale of phylogenetic relationships of closely related species 5‐kbp‐windows from the reference‐based pipeline and UCEs from the de novo assemblies are more successful than the BUSCOs in recovering informative markers for phylogenetic inference. Compared with concatenation analyses, coalescent analyses often resulted in disparate deeper relationships in the phylogeny. This study also uncovers evident mito‐nuclear discordance and demonstrates genome‐wide gene conflicts in phylogenetic signals, both pointing to possible incomplete lineage sorting and/or hybridization during the early, rapid radiation ofFormicaants. Divergence dating analyses show that different types of data and analytical methods could result in inconsistent time estimates, highlighting the potential need for multiple approaches to better understand species divergence. The strengths and weaknesses of different analytical pipelines and strategies are discussed. Findings from this study provide valuable insights for large‐scale phylogenomic projects using WGS data. 
    more » « less
  2. Abstract The ant genus Tapinoma Foerster, 1850 is a moderately diverse group (81 valid species) that occurs worldwide. It includes the tramp species T. melanocephalum, whose evolutionary history, biogeographic origin, and population limits remain unclear. Here, we present a time-calibrated phylogeny and a biogeographic history inference of the genus based on thousands of Ultraconserved Element (UCE) loci. Focusing on T. melanocephalum, we used single nucleotide polymorphisms from UCE loci and COI sequences to analyze species boundaries based on nuclear and mitochondrial DNA. We recovered a monophyletic Tapinoma with an estimated crown age corresponding to middle Eocene (49.4 to 34.4 Ma). Phylogenomic data differentiated T. melanocephalum from T. jandai, a recently established species based on morphology, and revealed that the 2 species diverged ∼12 Ma. Population genetic analyses identified considerable molecular divergence among sampled T. melanocephalum populations, and a heterogeneous genetic structure, showing a weak relationship between genetic differentiation and geographic distance. A phylogeographic comparison of habitat preferences of T. melanocephalum revealed an ecological shift from undisturbed to urban environments, a phenomenon which may have facilitated its ubiquitous and global distribution. Our study presents the first phylogenomic framework for this globally distributed ant genus and molecularly delineates a worldwide pest ant species. 
    more » « less
  3. Evolutionary adaptations for maintaining beneficial microbes are hallmarks of mutualistic evolution. Fungus-farming “attine” ant species have complex cuticular modifications and specialized glands that house and nourish antibiotic-producing Actinobacteria symbionts, which in turn protect their hosts’ fungus gardens from pathogens. Here we reconstruct ant–Actinobacteria evolutionary history across the full range of variation within subtribe Attina by combining dated phylogenomic and ultramorphological analyses. Ancestral-state analyses indicate the ant–Actinobacteria symbiosis arose early in attine-ant evolution, a conclusion consistent with direct observations of Actinobacteria on fossil ants in Oligo-Miocene amber. qPCR indicates that the dominant ant-associated Actinobacteria belong to the genus Pseudonocardia . Tracing the evolutionary trajectories of Pseudonocardia -maintaining mechanisms across attine ants reveals a continuum of adaptations. In Myrmicocrypta species, which retain many ancestral morphological and behavioral traits, Pseudonocardia occur in specific locations on the legs and antennae, unassociated with any specialized structures. In contrast, specialized cuticular structures, including crypts and tubercles, evolved at least three times in derived attine-ant lineages. Conspicuous caste differences in Pseudonocardia -maintaining structures, in which specialized structures are present in worker ants and queens but reduced or lost in males, are consistent with vertical Pseudonocardia transmission. Although the majority of attine ants are associated with Pseudonocardia , there have been multiple losses of bacterial symbionts and bacteria-maintaining structures in different lineages over evolutionary time. The early origin of ant– Pseudonocardia mutualism and the multiple evolutionary convergences on strikingly similar anatomical adaptations for maintaining bacterial symbionts indicate that Pseudonocardia have played a critical role in the evolution of ant fungiculture. 
    more » « less
  4. Abstract Many insect groups have acquired obligate microbial symbionts, and the resulting associations can have important ecological and evolutionary consequences. A notable example among ants is the species‐rich tribe Camponotini, whose members derive nutritional benefits from a vertically inherited bacterial endosymbiont,Blochmannia. We generate ultraconserved element (UCE) phylogenomic data for 220 ingroup and 5 outgroup taxa to reconstruct a detailed evolutionary history of the Camponotini, including the inference of divergence times and dispersal events. Under multiple modes of analysis, including both concatenation and species‐tree approaches, we recover a well‐supported backbone phylogeny comprising eight lineages: three large genera (Camponotus,Colobopsis,Polyrhachis) and several smaller genera or clusters of genera. Three novel lineages are uncovered that cannot be placed in any existing genus:Lathidrisgen. n., from the mountains of Mesoamerica;Retalimyrmagen. n., from the Indian Himalayas; andUwarigen. n., from eastern Asia. The species in these new genera were described and placed erroneously inCamponotus. The tribe Camponotini is estimated to have a crown origin in the Eocene (median age 38.4 Ma), with successively younger crown ages forColobopsis(22.5 Ma),Camponotus(18.6 Ma) andPolyrhachis(18.5 Ma). We infer an Australasian or Indomalayan origin for the tribe, with multiple dispersal events to the Afrotropics, Palearctic region, and New World. Phylogenetic analysis of selectedBlochmanniagenes from a subset of 97 camponotine taxa yields results that are largely congruent with the ant host phylogeny, at least for well‐supported nodes, but we find evidence thatBlochmanniafrom some old lineages—especiallyLathidris—may have discordant histories, suggesting possible lability of this symbiosis in the early evolution of camponotine ants. 
    more » « less
  5. Ruane, Sara (Ed.)
    Abstract Genome-scale data have the potential to clarify phylogenetic relationships across the tree of life but have also revealed extensive gene tree conflict. This seeming paradox, whereby larger data sets both increase statistical confidence and uncover significant discordance, suggests that understanding sources of conflict is important for accurate reconstruction of evolutionary history. We explore this paradox in squamate reptiles, the vertebrate clade comprising lizards, snakes, and amphisbaenians. We collected an average of 5103 loci for 91 species of squamates that span higher-level diversity within the clade, which we augmented with publicly available sequences for an additional 17 taxa. Using a locus-by-locus approach, we evaluated support for alternative topologies at 17 contentious nodes in the phylogeny. We identified shared properties of conflicting loci, finding that rate and compositional heterogeneity drives discordance between gene trees and species tree and that conflicting loci rarely overlap across contentious nodes. Finally, by comparing our tests of nodal conflict to previous phylogenomic studies, we confidently resolve 9 of the 17 problematic nodes. We suggest this locus-by-locus and node-by-node approach can build consensus on which topological resolutions remain uncertain in phylogenomic studies of other contentious groups. [Anchored hybrid enrichment (AHE); gene tree conflict; molecular evolution; phylogenomic concordance; target capture; ultraconserved elements (UCE).] 
    more » « less